**Bean Genome Diversity Reveals the Genomic Consequences of Speciation, Adaptation, and Domestication**

Andrés J. Cortés, Paola Hurtado, Mathew W. Blair and María I. Chacón-Sánchez

Additional information is available at the end of the chapter

http://dx.doi.org/10.5772/intechopen.80512

#### **Abstract**

Here we review whether genomic islands of speciation are repeatedly more prone to harbor within-species differentiation due to genomic features, such as suppressed recombination,- smaller effective population size, and increased drift, across repeated hierarchically nested- levels of divergence. Our discussion focuses on two species of *Phaseolus* beans with strong genepool and population substructure and multiple independent domestications each. We- overview regions of species-associated divergence, as well as divergence recovered in withinspecies between-genepool comparisons and in within-genepool wild-cultivated comparisons.- We discuss whether regions with overall high relative differentiation coincide with sections of- low SNP density and with between-species pericentric inversions, since these convergences- would suggest that shared variants are being recurrently fixed at replicated comparisons,- and in a similar manner across different hierarchically nested levels of divergence, likely as- the result of genomic features that make certain regions more prone to accumulate islands of- speciation as well as within-species divergence. We conclude that neighboring signatures of- speciation, adaptation, and domestication in *Phaseolus* beans seem to be influenced by ubiquitous genomic constrains, which may continue shaping, fortuitously, genomic differentiation- at various other scales of divergence. This pattern also suggests that genomic regions important for adaptation may frequently be sheltered from recombination.-

**Keywords:** genomic islands of speciation, genomic signatures of selection, adaptation, domestication syndrome, convergent evolution, gene flow, genomics constrains, GBS-derived SNP markers-

© 2018 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

### **1. Introduction: A strategy to discern among confounding causes of genomic divergence**

Genomic signatures associated with species, genepools, and ecotypes' divergence can result- from causes other than reduced gene flow, for example, random genetic drift and selection [1]. Moreover, the origin of the outlier variants from novel or standing genetic variation leads to distinctively different patterns of genomic divergence [2–4]. One approach that can help to distinguish- these underlying causes of divergence is carrying out a replicated sampling of contrasting populations [5, 6]. If genetic drift rather than selection is responsible for the divergence, it is unlikely that- signals of differentiation reappear consistently across replicates [5]. On the other hand, if selection- acted on the same genetic variants at the replicated contrasting pairs, genomic regions with comparatively high divergence between individuals from contrasting populations should be identical- at each of the replicated populations. Parallel selection on shared genetic variation should therefore lead to low divergence within populations and across replicates, in the exact genomic regions- where equivalent variants are selected at each contrasting population [6]. Discerning among gene flow, genetic drift and selection as the cause of parallel genomic divergence are possible as long as- there is some degree of replication considered in the sampling of contrasting populations.-

The genomic landscape of divergence can also be influenced by differences in ancestral variation and recombination in the genome [7, 8]. Lineage sorting may be enhanced relative to background levels by a reduction in the effective population size (N<sup>e</sup> ) due to processes other than gene flow, like low recombination [8–10]. Since differentiation is further speeded up in low-recombining regions because of linked selection [11–13], the imprint caused by genomic features on the differentiation landscape should be ubiquitous across different levels of divergence. Therefore, besides a replicated sampling of contrasting populations, a hierarchical nested sampling across various scales of divergence is advisable in order to examine whether genomic islands of divergence may display differentiation due to suppressed recombination, smaller effective population size, and increased drift.-

In order to discern among confounding causes of genomic divergence in a system with strong population structure and subjected to domestication, we suggest conducting the following analyses by taking advantage of a replicated hierarchical nested sampling across various scales of divergence:


Finally, we suggest exploring if regions of high FSTco-localized with regions of low FST in within-population comparisons. ΔDiv can be used to analyze the difference between these two values in each window. Peaks in the ΔDiv F statistic point to genomic regions that diverged ST- as a result of parallel divergence from shared variation rather than due to novel variation evolving at each site [6].

### **2. Beans as a model system to study divergence across various scales of divergence in a replicated hierarchical nested framework**

*Phaseolus* beans, with their striking genepool structure and multiple domestications, constitute an excellent model system [14, 15] to the approach described in the previous section and to explore to what extent genomic features, besides reduced gene flow and divergent selection, may lead to genomic divergence between (i.e., speciation islands) and within (i.e., during the natural colonization of new habitats as well as part of the domestication syndromes) species [16]. Common and lima beans are the only bean species with multiple domestications among the five domesticated species of *Phaseolus* [14]. Wild common bean (*P. vulgaris* L.) diverged from its sister species in the tropical Andes [17] and colonized South and Central America from its original distribution in Central America, originating what nowadays is known as the Andean and Mesoamerican genepools. Independent domestications in each genepool gave rise to the Andean and Mesoamerican cultivars [18–20]. On the other hand, wild lima bean (*P. lunatus* L.) diverged from common bean, after which natural spread also led to a strong genepool structure, with two Andean and two Mesoamerican genepools. Further independent domestications happened in one Andean and one Mesoamerican genepools [21].

With this in mind, in this chapter we discuss how the recurrent phylogeographic splits and nested domestication events of common and lima beans help understand whether genomic islands of speciation in *Phaseolus* species are more prone to harbor within-species divergence due to reduced recombination and increased drift (**Figure 1**). We concretely focus our discussion by asking the following questions:-


If there were some parallelisms in the genetic adaptations to the Mesoamerican and Andean environments or in the genetic consequences of the domestication syndromes, then there would be matching signals of differentiation in the within-species between-genepool divergence FSTprofiles and in the within-genepool wild-cultivated divergence FSTprofiles, respectively. These patterns of repeatability would not be observed if between-genepool and wild-cultivated divergence outliers were due to genetic drift [5], if selection pressures were different [22] or if equivalent selective forces did not act on the same shared variation [6, 23].

**Figure 1.** Schematic representation of a sampling across hierarchically nested sampling levels of divergence.

Yet, genomic constrains, rather than true signals of convergent adaptation and domestication, could still be the reason for these parallelisms. If genomic features were indeed constraining divergence, then genomic islands of differentiation would coincide with low-recombining regions regardless the nature and the scale of divergence.-

#### **3. Evidence that genomic features constrain divergence across scales**

By looking at the genomic diversity patterns in common and lima beans [24–30], there is evidence that differentiation across repeated and hierarchically nested levels of divergence always co-occurs with regions of low SNP density (**Figure 2**). Increased lineage sorting, and consequently rapid differentiation, is a common phenomenon in low-recombining regions because of linked selection and a reduction in the effective population size [8–10]. Likewise, low-recombining regions also tend to exhibit a decline in diversity due to background selection and, to a lower extent, because of genetic hitchhiking [11]. This can be understood as evidence that regions with low SNP diversity are enriched for contiguous signatures of differentiation between bean species, between genepools, and as part of the multiple domestication syndromes. These concurring signatures could be a by-product of genomic constrains inherent to low-recombining regions.

One of the regions that repeatedly exhibit high differentiation across hierarchically nested levels of divergence in the presence of low SNP density is the centromeric section of chromosome Pv11. The wild-cultivated divergence peak in this chromosome is shared by three domestication syndromes and is located beside the outlier peak detected for all within-species between-genepool comparisons, which in turn coincides with a major between-species peak. In this wide section of chromosome Pv11, there are indications that convergent divergence is consistently correlated with very low SNP density, as expected because of combined effects of linked and background selection in low-recombining regions [8–10, 22]. The observation that genomic constrains are biasing divergence across scales in this section of chromosome Pv11

Bean Genome Diversity Reveals the Genomic Consequences of Speciation, Adaptation, and Domestication 31 http://dx.doi.org/10.5772/intechopen.80512

 **Figure 2.** Patterns of genome-wide diversity in common bean and lima beans based on 13,213 GBS-derived SNP markers. A sliding window analysis (window size-=-1 × 107 bp, step size-=-500kb) was used to compute (**A**) SNP density, (**B**) nucleotide diversity as measured by π, and (**C**) Tajima's D.-Vertical translucent boxes highlight the 1-Mb flanking region of each FST-based outlier window midpoint when FSTwas computed as follows: (**red boxes**) between species (*P. lunatus*  versus *P. vulgaris*), (**gray boxes**) between genepools (average of four within-species between-genepool comparisons), (**green boxes**) between domestication statuses for *P. vulgaris* (average of two within-genepool wild-cultivated comparisons), and (**blue boxes**) between domestication statuses for *P. lunatus* (average of three within-genepool wildcultivated comparisons). Results of all windowed analyses are plotted against window midpoints in millions of base pairs (Mb). Black and gray colors highlight different common bean (Pv) chromosomes. Gray arrows on the vertical axes indicate genome-wide averages. Horizontal gray lines with a central-filled gray dot at the top of the figure mark the centromeres [from 20] (figure modified from [16]).

is reinforced by the fact that previous genomic scans did not attribute to this region a consisted outstanding role during the domestication syndromes [20, 21] or in conferring adaptation to different environments and latitudes across the Americas [31]. The only exception is the candidate gene influencing plant size (*Phvul.011G213300*) as part of the Mesoamerican domestication syndrome of common bean [20], but then this pattern has not been consistently reported for the other domestication events as to explain its steady repeatability across hierarchically nested levels of divergence in windows with low SNP density.

Other "hotspots" for spurious divergence due to genomic constrains may be the regions with low SNP density in chromosomes Pv8 and Pv10 that exhibit signatures of between-species divergence as well as repeated between-genepool and within-genepool wild-cultivated divergence (**Figure 2**). The region in chromosome Pv8 was previously reported to be highly divergent during the domestication of the Andean common bean, but then there were not candidate genes in this region associated with that domestication syndrome in particular [20], despite that the same region is known for being involved in plant and seed growth (i.e., *Phvul.008G168000*) during the Mesoamerican domestication of the same species. This paradox may then be a consequence of genomic constrains obscuring genuine anthropic selection and repeatedly forcing divergence in this region. Similarly, the wide divergent region in chromosome Pv10, characterized by two outlier peaks split by a "high valley," actually matches a pericentric inversion between species [32], exemplifying how genomic features inexorably condition differentiation across scales of divergence.-

The observation that low-recombining regions are enriched for differentiation across repeated- and hierarchically nested levels of divergence in *Phaseolus* beans opposes the profiles of the- genome-wide selection scans carried out in common bean. While low-recombining regions are- more prone to exhibit signatures of divergence, regions toward the arms of the chromosomes- with high SNP density more often harbor adaptive variation [31]. This trend follows expectations because low-recombining regions are more liable to display divergence because of linked- selection [11, 33, 34], whereas recombination hotspots usually exhibit higher SNP density and- are enriched with functional genes [11, 35]—an already well-described relationship for common bean [36, 37]. Also, adaptive divergent selection usually homogenizes haplotypes within the- same niche and fixes polymorphisms in different populations, so that few haplotypes with high- frequency remain. This selective process leads to high values of nucleotide diversity and Tajima's- D and low values of the Watterson's theta (θ) estimator [38], a tendency that was corroborated in- wild common bean when looking for adaptive variants [31] but that was lacking in the present- study while retrieving the genomic landscape of divergence between species, genepools, and- domestication statuses.-

#### **4. Signatures of shared within-species parallel divergence**

There is some evidence of some parallelisms in the genetic adaptations to the Mesoamerican and- Andean environments in common and lima beans (**Figure 2**). The landscape of genomic adaptation has remained largely unexplored in *Phaseolus* beans. Among the few other studies addressing this question, a panel of wild common bean sampled across the Andean and Mesoamerican- ranges revealed that regardless the strength of the bottlenecks [39], the signatures of divergent- adaptation are widespread along the genome and coincided with regions of elevated SNP density [31], frequent recombination, and high gene content [36]. However, these surveys have not- explicitly addressed the colonization of the Andes by linages coming from Central America and- the corresponding change in selection pressures associated with different altitudes, latitudes,- and microenvironments. Topographically complex mountainous systems, such as the Andes,- harbor an impressive heterogeneity of climates at a small scale [40–43]. The ridges and valleys- constitute physical barriers that limit dispersal and cause local variation in rainfall, resulting in- genetic isolation and variation in habitats. Both processes have likely speeded up the evolution- of high species diversity in this region [44–48]. Yet, the relative effects of geographic isolation- [49–51], environmental variation at a small scale [52–58], and their potential interactions across- genepools remain poorly understood in wild beans. Therefore, characterizing the genomic- consequences associated with the colonization of heterogeneous environments may ultimately- disclose further cases of genetic parallelism in the adaptation of beans.-

The genomic consequences of multiple domestication events are also moderately recurrent asrevealed by our survey. From the twelve regions putatively differentiated as the result of thedomestication syndrome, only five (42%) appear in more than one comparison but none appearsin all. Two peaks in chromosome Pv3 and Pv10 are repeated across three different comparisonsof all five profiles of the domestication syndromes. At least the region in chromosome Pv3 has- been reported to be involved in the vernalization pathway (i.e., *Phvul.003G033400*) as part of the Mesoamerican domestication of common bean [20]. Two other divergence peaks in chromosomes Pv8 and Pv11 are consistent across all three genomic profiles of the Mesoamerican- domestication syndrome. The region in chromosome Pv8 is known for being related with the- encoding of the nitrate reductase (i.e., *Phvul.008G168000*), a critical element for plant and seed- growth, during the Mesoamerican domestication of common bean [20]. Also as part of this domestication event, the region in chromosome Pv8 is associated with increased plant size- through the ubiquitin ligase degradation pathway (i.e., *Phvul.011G213300*) that controls flower- and stem size [20]. More loosely, a peak at chromosome Pv2in the Mesoamerican common- bean domestication FSTprofile is recovered in the profiles of all three lima bean domestications. This region has been linked with the domestication syndrome of lima bean since it is- involved in the regulation of seed germination (i.e., *Phvul.002G033500*) and leaf size (i.e.,- *Phvul.002G041800*) and is enriched by inflated linkage disequilibrium scores [21]. Although- scattered, some of these few regions may reveal true parallelisms in the domestication syndromes, whereas others may still be constrained by genomic features.-

Also striking is the rarity of regions putatively involved in domestication and shared by several domestication events. This trend, mostly expected for quantitative traits with complex genetic architectures [59–61], had already been noticed for the common bean [20]—potentially applying for lima bean as well [21], and so does not necessarily speak for a prevalent role of drift. Since divergence in the lack of repeatability is a liable result of lineage sorting, caution must be undertaken while interpreting these signals. Singularities may result from different adaptive pressures across the Americas unique to each species, distinctive adaptation to the Mesoamerican microenvironments, dissimilar selection as part of each domestication event [22], equivalent selective forces acting on different genetic variants [6, 23], or genetic drift [5]. Discerning among these causes requires further genotyping in an extended panel specifically addressing each comparison. At least for the divergence peak at chromosome Pv7in the wild-cultivated Mesoamerican common bean comparison, other drivers besides the domestication itself are an unlikely reason for divergence because a wide region in chromosome Pv7 region is known for being associated with increased seed weight (i.e., *Phvul.007G094299*- *Phvul.007G.99700*) during the Mesoamerican domestication of common bean [20], as well as with flowering regulation (i.e., *Phvul.007G096500* and *Phvul.007065600*) as part of the domestication of lima bean [21] and both common bean genepools [20].

#### **5. Take-home message**

Genomic islands of speciation are not necessarily more prone to harbor within-species divergence, yet subjacent genomic constrains could still be shaping parallel divergence at broader- genomic scales. With that in mind, we first discussed how genomic features and linked selection could enhance convergent differentiation in low-recombining regions. Later, we reviewed- cases of moderate repeatability in the genomic consequences of multiple adaptation and domestication events. This chapter emphasizes that differentiation across repeated and hierarchically- nested levels of divergence co-occurs with regions of low SNP density, and these concurringsignatures may be a by-product of genomic constrains inherent to low-recombining regions.- We advise a more systematic use of repeated and hierarchically nested samplings in order to- improve our understanding of the underlying causes of the genomic landscape of divergence.- Because certain regions are more prone to accumulate islands of divergence as the result of- genomic constrains, we advocate that studies of genomic divergence should consider more- systematically a dual-purpose sampling, such as the one we described in the first section. In the- first place, using replicated populations under presumably similar selection pressures helps- accounting for lineage sorting and characterizing the nature of the selected variants, i.e., novel- versus standing [6]. Second, a hierarchically nested sampling across various levels of divergence allows for further assessments on the processes, which like genomic constrains, may- give rise to parallel divergence patterns [2–4, 62]. Finally, some of these examinations must- be verified with genomic features and estimates of the recombination rate [63–65]. We foresee- that as the evidence of pervasive genomic constrains shaping genomic differentiation across- species and at countless scales of divergence accumulates, replicated samplings of contrasting- populations in a hierarchically nested framework of divergence will become indispensable.-

In the long run, we are looking forward to see more coherent and systematic samplings of replicated contrasting populations across hierarchically nested levels of divergence in of genomic- divergence has always been challenging, but the field is now moving forward toward a more- cohesive framework. New ways [66, 67] to characterize obscuring genomic features promise- aiding our understanding on how the genomic landscape of divergence is shaped.-

Among the five domesticated species in the *Phaseolus* genus, common and lima beans are- the only ones exhibiting range expansions toward South American and multiple domestications [14]. However, exploring the landscape of divergence in other domesticated *Phaseolus*  species is equally insightful because of their overlapping distribution ranges, nested phylogenetic relationships, and divergent adaptations. For instance, year (*P. dumosus*) and runner- (*P. coccineus*) beans are Mesoamerican and well adapted to humid habitats, which makes- them a potential source of resistance to biotic stresses. On the other hand, tepary bean (*P. acutifolius*) is also Mesoamerican but is well known for growing in desert and semiarid- environments, which makes it a likely source of tolerance to abiotic stresses. These species- also possess well-established genomic resources [68] that could speed up newer genomewide comparisons. *Phaseolus* species that never underwent domestication are also abundant (ca. 70) and could enrich our understanding of genomic divergence in this intricate- complex. Considering the *Phaseolus* species complex as a whole will ultimately reinforce- beans as a model for understanding speciation, adaptation, and crop evolution [14, 15, 69–72].

#### **Acknowledgements**

 Some of the ideas presented in this chapter were refined thanks to the comments from A.-Caro,- I.-Cerón, C.-Jiggins, D.-Londoño, P.-Reyes, C.-Salazar, J.J.-Wiens, and R.-Yockteng during the- VI Symposium of the Colombian Society for Evolution held in Cali (Colombia) on August 2017.- This chapter was funded by a Colciencias (Colombia) grant awarded to MC under contract- number FP44842-009-2015 and project code 1101-658- 42502, by the grant 3404 from Fundaciónpara la Promoción de la Investigación y la Tecnología del Banco de la República de Colombia to- MC, and by the Lundell and Tullberg (Sweden) grants to AC.-The Geneco mobility fund from- Lund University is thanked for subsidizing the meeting between AC and MB in the spring of- 2015 at Nashville (TN, USA). AC's writing time was sponsored by the grants 4.1-2016-00418- from Vetenskapsrådet (VR) and BS2017-0036 from Kungliga Vetenskapsakademien (KVA). MB- received support from the Evans-Allen fund of the US Department of Agriculture. The editorial- fund from the Colombian Corporation for Agricultural Research is acknowledged for financing- this publication.-

### **Author details**

Andrés J.-Cortés1,2\*, Paola-Hurtado3,4, Mathew W.-Blair<sup>5</sup> and María I.-Chacón-Sánchez<sup>3</sup>

\*Address all correspondence to: acortes@agrosavia.co

1 Corporación Colombiana de Investigación Agropecuaria (Agrosavia), Rionegro, Colombia

2 Universidad Nacional de Colombia - Medellín, Facultad de Ciencias Agrarias - Departamento de Ciencias Forestales, Medellín, Colombia-

3 Universidad Nacional de Colombia -Facultad de Ciencias Agrarias - Departamento de Agronomía, Bogotá, Colombia-

4 Department of Plant Sciences, University of California, Davis, California, USA-

5 Department of Agricultural and Environmental Science, Tennessee State University, Nashville, USA-

#### **References**


## **Induced Mutation: Creating Genetic Diversity in Plants**

Kamile Ulukapi and Ayse Gul Nasircilar

Additional information is available at the end of the chapter

http://dx.doi.org/10.5772/intechopen.81296

#### Abstract

Genetic diversity is the variation occurred in genetic information, which depends on frequency and diversity of alleles among individuals within a population or a species. This phenomenon, which is also a part of the evolution process, allows the organisms to adapt to changing conditions and to survive. Populations with high allelic variability are more easily adaptable to changing environmental conditions. However, nowadays, constant use of populations with certain characters in the plant breeding and the uniformity of consumer demands are among one of the causes of genetic erosion. Loss of genetic diversity within a species can lead to loss of useful properties for human beings. If stress conditions such as disease or drought occur, the ability of a population to survive by adapting to this new condition is dependent on the presence of individuals carrying gene alleles that need to adapt to these conditions.

Keywords: gamma rays, genetic diversity, induced mutation, plant

#### 1. Introduction

The first information on the importance of genetic diversity begins with Darwin, which emphasizes the importance of variations in the process of adaptation to natural habitat. In the process of surviving species that can adapt to changing environmental conditions and the disappearance of others, the factors that caused them were researched and the definition of alleles was first used by Mendel, who is considered the father of heredity. Alleles do not only create the source of similarities and differences between progenies, but also makes it possible for species with high genetic diversity to continue their evolutionary process by adapting to different conditions. A biochemical approach to genetic diversity was presented by the introduction of isoenzyme techniques in the mid-1960s. In the following years, the discovery of the structure of DNA and its DNA-based examination of diversity has enabled scientists to reach

© 2018 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

accurate information about genetic diversity, gene flow, and the origins of species. According to the "Neutral Theory of Molecular Evolution" first introduced by Motoo Kimura in 1968, many of the evolutionary changes arise from the genetic drift of the neutral mutant alleles. Greater than 100 bp insertion/deletion is rapidly removed by natural selection that has caused a great change and damage to the DNA. According to the neutral hypothesis, mutations that occur with smaller changes are harmless mutations. They are protected in the evolutionary process by contributing to the formation of genetic diversity. Most of the polymorphisms are kept in a population by mutation and random genetic drift [1–7].

The genetic difference between individual of a species is the basis for evolution and adaptation. If all of the individuals were genetically identical, species could not be survived under changing environmental conditions such as drought and salinity. It is known that there is a positive correlation between fertility and viability with population size and genetic variation. For this reason, regardless of whether the existing genetic diversity is beneficial, it should be considered that it poses a potential against rapidly changing environmental conditions [8, 9]. Loss of genetic diversity will adversely affect the ability to deal with environmental change in the evolutionary process. It is anticipated that, particularly small and isolated populations will be more affected by this loss [4]. Although loss of genetic diversity has been thought to be a threat to rare species for a long time, it has also been found to be effective on widespread species with large populations [4, 10, 11]. Furthermore, the fertility and viability rate of populations with reduced genetic variability and loss of valuable alleles, especially as a result of self-destruction, is diminishing. Random genetic drift changes the frequency of alleles between generations. The frequency of some of the alleles may decrease while the other allele may become more common. Naturally occurring mutations also support this process. The genetic variation among individuals is the basis for the evolutionary change of species, populations, and progeny. Evolutionary change requires modifications of genes or gene combinations. The functions of the existing alleles are altered by mutation or recombination. Appropriate mutations can help the organism better use the current environment. Alleles that are previously neutral or have little effect on the reproduction success of individuals may suddenly become important. Obtaining useful genetic variations through natural mutations is a very slow process. In the future, it is impossible to predict which alleles will be necessary for a survival. For this reason, populations and species with high genetic variation are more likely to have alleles that may be necessary for adaptation to changing conditions. Generally, natural populations have the variation to be expressed in the case of the change of selection pressure. The basis of plant breeding is also based on this genetic variation. By artificially altering the selection pressure, some alleles come forward and populations gain new features. Since there is a positive correlation between population size and genetic diversity [12], decreasing population size or limiting gene flow between subpopulations may cause a reduction in genetic diversity [13]. Genetic drift with a positive role in the evolutionary process [3], inbreeding, mating between close relative individuals, reduction of viability and fertility of individuals in the population may cause effects such as the reduction of heterozygote, allelic losses, and some alleles become fixed in the population. As a result, genetic variation will be lost in populations [9, 12, 14]. Many populations are so small that genetic drift, a random process, has an important influence on the number of alleles that will be transferred to future generations. The useful alleles transferred from previous generations may be lost as a result of genetic drift [1]. Two main consequences of genetic drift; (a) different alleles frequencies between generations are irregular and (b) the genetic diversity of the populations is lost. At the beginning, rare alleles will disappear and the mean heterozygote will decrease over time. While genetic diversity within populations decrease, genetic differences between populations may increase or decrease depending on whether the random genetic drift in different populations in the same or opposite direction. This loss will continue until the gene pool is stabilized for an allele or until a balance is established between loss of genetic variation and genetic variation through mutations. The loss of both rare alleles and heterozygotes, which cause the decrease in genetic diversity in the population, will decrease in an inverse proportion to the effective population size (Ne). The population size (Ne), which helps to determine the demographic structure of the population, makes it possible to predict the change in genetic diversity. Population size is an important factor that increases the genetic diversity of individuals' intra-species and between taxa. Besides genetic diversity of non-endangered species is higher than endanger species [6, 15–17]. Only a small amount of gene flow may be sufficient to prevent the loss of genetic diversity in a population. Especially, the accumulation of mutations with small deleterious effects in the alleles may reduce the viability and fertility of the populations. These mutations never reach high frequencies in large populations of sexual reproduction. The selection pressure prevents these harmful alleles to become widespread. However, in isolated small populations, the frequency of these harmful alleles may increase and be fixed by chance, if genetic drift may be stronger than natural selection. When a harmful mutation is stabilized in the genetic construct, it causes the population size to decrease and other harmful mutations to be fixed [18]. While the destructive effect of detrimental mutations affect large populations, thousands of years later, can be seen in minutes in small populations. This event, known as mutation meltdown, reduces the size of the population depending on the accumulation of detrimental mutations. The mutation meltdown, is a genetic problem, especially for small populations of endangered species, occur depending on mutation characteristics, demographic characteristics of the mutation and population, and the relationship between mutations and their adaptation [19, 20]. Species or populations suffering from the genetic bottleneck disappear over time. Adaptation can sometimes be a rapid process involving a single gene. In cases when the positive selection is strong, the best allele is fixed in the relevant locus and the adaptation process is terminated unless a better allele is generated by mutation or a new allele is introduced into the population by gene flow. This does not occur in polygenic characters. Genetic drift has a significant impact on the protection of genetic diversity and the amount of genetic variation among populations. Genetic drift as well as mutations, selection, and gene flow are factors contributing to genetic diversity. Sometimes, however, subspecies can occur as a result of gene flow, and which can adversely affect fertility or cause outbreeding depression [9, 21].

#### 2. Natural mutagenesis

When damage occurs in DNA due to a physical, chemical, or biological agent, molecular systems recognize and repair this damage. When this mechanism is unsuccessful, mutation occurs in the organism [22]. Mutagenesis, a consequence of errors in DNA repair, is a mutation-producing process. Hereditary changes that occur naturally and suddenly, which are not caused by recombination and segregation, are called mutations [23]. Mutations that lead to the formation of new individuals, species, and genera are considered as the most important factors of evolution since they can be transferred to future generations [24]. Mutations that occur in somatic cells are not transferred to future generations, but they are important for vegetative produced species. Mutation-derived individuals are called "mutants" [23]. Natural mutants formed in the evolutionary process are one of the most important factors contributing to the formation of species. The rate of spontaneous mutations in higher plants is quite low (10˜<sup>5</sup> –10˜<sup>8</sup> ) [25]. Mutations occur more frequently in some regions of the genome. For example, in almost all organisms, the mutation rate in GC regions is higher than in AT regions [26]. While deleterious or neutral mutations that form a part of the mutations that occur in the natural process may disappear in the evolutionary process, the protected mutants may have desirable agricultural characteristics or easily adapt to changing environmental conditions [25]. The first document relating to mutant selection belongs to the year 300 BC. The description of various wild and cultivated mutants was made by Linnaeus in the second half of the 1700s [23]. Although hereditary variations have been observed and used for thousands of years, the mechanism of heredity was first revealed by Mendel [27]. Johanssen's research on seed index of common beans in 1913 can be considered as the first to prove the presence of natural mutations with small effects. In 1924, Baur emphasized that the accumulation of these small mutations in the genome over the years had an impact on the evolution process [28]. Mutation term was first used by de Vries at the beginning of the 1900s. The first evidence of mutation breeding work, which will gain a new perspective on plant breeding, was obtained in 1927 in Datura stramonium by radium ray application [20]. The process that begins with human being's awareness of natural mutation has led to the development of many new varieties with induced mutation.

Mutations can occur in spontaneously or under different influences of various mutagens. For this reason, there are various classifications made by different researchers [2, 29–33]. Yüce et al. [34] classified mutations into two main categories as genomic and plasmon mutations. Genome mutations; (1) "gene mutations" resulting from genetic changes, (2) "Chromosomal mutations" formed by chromosome aberrations or chromosomal changes, (3) "Ploidy mutations" resulting from genome and chromosome number changes, (4) Mutations created by transposition elements, and (5) Mutations resulting from somaclonal and gametoclonal variations were classified as five subgroups. Mutations occurring in the genetic material of mitochondria and plastids in the cytoplasm are classified as "plasmon mutations" in a single heading [34].

Gene mutations are structural gene changes in DNA that occur through different mechanisms such as deletion, insertion, and substitution. Intercalar substances, ultraviolet rays, alkylating compounds, and free radicals cause gene mutations [33, 34].

Chromosome mutations are genetic changes that are generally caused by deletion, duplication, inversion, and translocation mechanisms and are larger than gene mutations [33, 34].

Ploidy mutations are divided into two main groups as polyploidy and aneuploidy. The smallest ploidy level is the haploid in the gametes, containing n chromosomes. Eukaryotes contain diploid (2n) chromosomes in cell nuclei. Cells that contain more than two genomes in the nucleus are called polyploids. Polyploidy are very common in plant kingdom and are naturally seen in important cultivated plants such as wheat, cotton, potato, banana, and coffee. These species, which contain more than two alleles in terms of genetic structure, display a richer genetic variability. Aneuploidy is the number of chromosome changes that occur as an increase or decrease in the number of chromosomes. In this case, individuals with fewer or more chromosomes than normal chromosomes are formed [34, 35].

Transposon elements are the mobile genetic elements found in the genome and cause mutation due to their ability to displace within the genome [36, 37].

Somaclonal and gametoclonal variants, another source of mutations, are genotypic or phenotypic differentiations in somatic or gametic cells, which are formed by hormones used in tissue culture media [34, 38, 39].

Spontaneous mutations caused by disruptions in the functioning of molecular mechanism in the cell, the main source of genetic diversity [40]. In every generation, 10˜<sup>5</sup> –10˜<sup>6</sup> mutation rate per gamet cell occurs. This ratio can vary between genes and even by regions within the genes [41]. Although mutations occur infrequently, when considered as a whole genome, it plays an important role in the change of genetic diversity. Because mutations occur at randomly, and it cannot know which one of the gene copies will mutate in diploid or polyploid organisms [22].

Spontaneous mutations have been the basis for the beginning of agriculture and for humankind to pass on a settled life. Self-changing hereditary features have made the dormancy period reduced in species such as peas, wheat, and barley. In addition, the loss of bitterness was formed in almond, linden, watermelon, potato, eggplant, cabbage, and various hazelnut species. All these developments have made these products suitable for human consumption. Another spontaneous mutation was the formation of parthenocarpy in grape and banana (Table 1). Naturally occurring mutations have led humans to work on induced mutations [42].


Table 1. Useful properties acquired by spontaneous mutations in evolutionary processes in plants (Table was directly taken from Mba [42]).

#### 3. Induced mutation

When it considered the changing environmental conditions and population growth, it is necessary to increase agricultural products approximately 70% in near future [43]. However, breeding trials for the development of desirable agricultural characteristics cause genetic bottleneck. Genetic resource erosion in plants will also lead to the loss of useful genes that would potentially create for breeding studies [44]. Induced mutations may help regain lost traits due to reasons, such as stress factors in the evolutionary process. These genotypes, exempted by the ethical and legal limitations faced of genetically modified products, can be identified by advanced molecular techniques. Thus, the variation of the mutants with the new phenotypes revealed can provide a different perspective for plant breeding studies [45]. Mba et al. [46], referring to the importance of landrace and wild varieties as important genetic resources in breeding strategies, proposed that artificial mutation of putative parental materials in order to create new alleles controlling the desired characters for the twenty-first century "smart" crop varieties [42].

There is a 125-year history of studies on induced mutation. It was determined that X-ray, alpha, beta, and gamma rays are the source of radiation, with different studies in 1895–1900. In 1897–1908, the first studies were carried out to investigate the effects of radiation on plants in 1901 and 1911, it is proved that mutation was induced by chemicals at the first time. In 1904 and 1905, Hugo de Vries suggested that radiation promoted artificial mutation. In 1910, Thomas Hunt Morgan did his first mutation experiments with Drosophila melanogaster. In 1927, Muller proved precisely that the X-rays induced mutation. In 1928, Lewis John Stadler successfully induced mutation in corn and barley using X-rays. In the years 1934–1938, Tollenar improved the first commercial variety of tobacco called "Chlorina," and this variety was released in Indonesia [28]. After these initial developments, the curiosity and research of the scientists against the induced mutation have continued.

Today, there are 3222 commercial mutant varieties according to the IAEA data. The countries where the most mutant species are released are China (810), Japan (481), and India (330). According to this data, the highest mutant cultivation rate is in Asia continent [47]. When the products are examined, the percentage of mutant varieties by mutation breeding are constituted of 49.5% cereal, 21.9% ornamental plants and flowers, 15% legume, 2.4% fruit nuts, 2.4% vegetable crops, 2.3% fiber crop, 2.1% oil crops, 1.2% forage crops, 0.6% root-tuber crops, 0.4% herbs, 0.2% medicinal plants, and 2% other crops [48].

Mutations can be induced by biological, chemical, or physical factors as well as spontaneous [40]. In breeding studies, physical and chemical mutagens are generally preferred, but mutations also can be generated by biological agents such as viruses and bacteria. While X-rays, γrays, fast neutrons, ultraviolet (UV) rays, beta particles, alpha particles, protons, and ion beams are used as physical mutagens, as chemical mutagens; alkylating agents, azide, hydroxylamine, antibiotics, nitroso compounds, acridines, and base analogs are used for mutagenesis [32, 47]. However, "insertional mutagenesis" and "site-directed mutagenesis" methods, which give more precise results in parallel with progress in genome and sequencing studies, are predicted to be used more widely in future mutation breeding studies [49, 50]. Mutant plants were mostly developed using physical mutagens. Physical mutagens are preferred to chemical mutagens for reasons such as ease of use, low cost, and nontoxicity. In particular, gamma and X-rays are the most commonly used mutagens. About 64% of the mutant plants obtained with the physical mutagens were improved using gamma rays [51–53].

Different plant parts such as seed, meristem, callus, and anther can be used in induced mutation studies. Mutation studies begin with the initial phase, called M0, where different plant materials are used. Each generation of the mutation continues in the form of M1, M2, M3,…. When a seed is used as the starting material, homohistont generation is obtained at the M2 stage, while the number of cycles may increase in mutagenesis using vegetative tissues. Screening and selection starts with the first homohistont generations. Once these stages are completed, experiments are carried out to release the mutants obtained, or they can be used as parents in breeding programs [23].

### 4. Use of induced mutations in the enrichment of plant genetic resources

Induced mutation studies were initially conducted only in field conditions. Tissue culture studies, began with cell culture at the beginning of the twentieth century, have become widespread parallel to the development of technology and have enabled the rapid and disease free reproduction of many plant species. In vitro mutation may be preferred for tolerance selection, especially for stress and diseases, because of the shortening of the selection period, being economical and the need for small areas in the mutation studies. Generally, plants are transferred to field conditions after the selection made in step M1V3 in vitro and in this way provides the researcher time and labor savings.

In vitro and in vivo conditions, different plant explants and different doses of the mutagen to be administered have used to create variations in plant species. High dose applications will increase mutation frequency in induced mutation studies to create genetic diversity in plants. In this case, however, the percentage of survival of the plants will either be too low or the plant will die [54, 55]. For this reason, appropriate dose determination is required for each mutagen and plant species. Appropriate dose determinations are made on the basis of M1 plants survival rate and vegetative growth, primarily shoot height [56]. A sample graph, appropriate doses calculated according to survival rate of some common bean cultivars by gamma irradiation are given in Figure 1 [57].

Numerous studies have been carried out for enriching genetic variation by plant-induced mutation and using this variation to the benefit of humankind (Figure 2). Some of these studies were conducted in order to create polymorphism by removing genetic bottleneck. In this way, new hybrid groups can be formed. Genetic diversity is also important for breeding programs and the sustainable use of genetic resources [58]. Genetic variation obtained from induced mutation has contributed to modern plant breeding. Studies conducted by mutation breeding can be summarized under the titles of biotic and abiotic stress tolerance, improving plant nutritional properties, and increasing polymorphism. Barakat and El-Sammak [59] in Gypsophila paniculata L., Kaul et al. [60] and Barakat et al. [61] in chrysanthemum obtained mutant

Figure 1. Stages of mutation breeding (Figure was directly taken from Jankowicz-Cieslak et al. [27]).

Figure 2. LD50 values of two common bean cultivars (figure was directly taken from Ulukapi and Ozmen [57]).

plants and they identified mutants' genetic similarity with molecular markers (from 0.59 to 0.97, 0.06 to 0.79, and 0.43 to 0.95, respectively). About 83% polymorphism was detected in the chrysanthemum as a result of gamma-induced mutation. It has been reported that the 30 Gy gamma dose is the most effective dose for in vitro genetic variation [62]. Wu et al. [63] have developed resistance at varying frequencies to blast, bacterial blight, and tungoric disease using both chemical (diepoxybutane and ethylmethanesulfonate) and physical (fast neutron and gamma ray) mutagens in rice. The semidwarf rice mutant "Calrose 76" released in California and the short height mutant rice called "Basmati 370" in Pakistan were improved [64]. EMS is the most preferred chemical mutagen. It causes a single nucleotide polymorphism (SNP). In this way, even a single change in the genomic coding sequences will change the expression of the gene, causing changes in transcription and translation products [65]. Till et al. [66] developed two mutant rice populations using ethyl methanesulphonate (EMS) and a combination of sodium azide plus methyl-nitrosourea (Az-MNU). The investigators have screened target genes and identified 30 nucleotides changes in Az-MNU population and 27 nucleotides in the EMS population. In a study using EMS as a chemical mutagen, four populations with different mutation densities were developed on soybean. The results are described by Targeting Induced Local Lesions IN Genomes (TILLING) [64]. Minoia et al. [68] obtained a new mutant collection at domestication by EMS. All of the genome scans identified 66 nucleotide substitutions and reported two different mutation intensities. In Barley, two gene-induced mutations were generated using EMS and the results were confirmed by sequence analysis [69]. In another study conducted at barley, 63 androgenic doubled-haploid mutants were obtained by sodium azide application during anther formation in vitro [70]. In the study by Kim et al. [71], homologous mutant lines were developed resistant to 5 methyltryptophan (5MT) in rice. In a similar study in rice, mutants which were resistant to 5 methyltryptophan (5MT) were also developed, and the amount of both protein and nine free essential amino acids increased significantly from the original variety [72]. In another study on rice, a new mutant genotype with high tocopherol content was obtained in in vitro mutagenesis with gamma irradiation. Mutant individuals were found to have higher seed viability than the control group and seedling growth was faster in the early growth phase [73]. Induced mutation treatment resulted in acidity and drought tolerance in lentil and rice [74–76]. Again, in a study of rice, salt tolerant varieties were obtained by mutation induction [77]. As seen in all of these studies, many mutagenesis applications have been made in order to improve plant characteristics and to create genetic diversity, and successful results have been achieved. Some methods are used to detect the regions of mutation and density. Methods such as conformation-sensitive capillary electrophoresis (CSCE), single-strand conformation polymorphism (SSCP), and denaturing high performance liquid chromatography (dHPLC) are used to determine variations in plant genes. In addition to these methods, TILLING and Highresolution melting (HRM) are used to determine the induced polymorphism [25, 65, 67].

#### 5. Conclusion

Mutations naturally occurring in the evolutionary process led to the formation of new genotypes. Mutations that occur in nature spontaneously have been modeled for humankind in order to increase the genetic diversity, which is narrowed as a result of natural selection and classical breeding studies. Thus, induced mutation studies have begun. Mutation induction studies, which provide new alleles to the genome by different methods, contribute to the increase of genetic diversity. The increase in genetic variation will increase the chance of survival of species in changing biotic and abiotic conditions. Genetic diversity is not only important for the continuity of species, but also improves the quality criteria of plants, which are raw materials of many industrial products such as food, pharmaceutical, textiles, etc., in these sectors.

#### Conflict of interest

The authors declare that they have no conflict of interest.

#### Author details

Kamile Ulukapi<sup>1</sup> \* and Ayse Gul Nasircilar<sup>2</sup>

\*Address all correspondence to: kamileonal@akdeniz.edu.tr

1 Vocational School of Technical Sciences, Akdeniz University, Antalya, Turkey

2 Department of Mathematics and Science Education, Faculty of Education, Akdeniz University, Antalya, Turkey

#### References


**Chapter 5**

Provisional chapter

**Water and Ecosystem Cycles Mediated by Plant Genetic**

DOI: 10.5772/intechopen.79781

Plant genetic resources for food and agriculture play essential roles in sustainable development and the conservation of global biodiversity. Especially, water cycle and related material circulation are deeply influenced by the loss of plant species diversity and external inputs through agricultural practices. This chapter overviews the water and ecosystem cycles mediated by the ecosystem functions of naturally occurring plant communities and discusses possibilities for the transformation of agriculture into sustainable modality with the primary importance on the recovery of water cycle. The transformation requires an intensive utilization of plant genetic resources in various ways compatible with a multiscale integrated model of water and material cycles based on the processes of ecological succession and evolution. This foresight sheds light on the new importance and utility of plant genetic resources for food and agriculture, in the face of climate uncertainty and in

Keywords: water cycle, material cycles, biodiversity, ecosystem functions, plant genetic

An abundant water cycle supports the ecosystem in the world we live in. Without water filling the earth's surface and flowing back to it, life would not have reached dry land and flourished. Water is the most important substrate for life. The underground water permeating the soil, the rivers flowing through the earth's surface, the lakes creating lush landscapes, and other components of the dynamic water cycle are all supported by the activities within the ecosystem. This chapter looks at the interactive relationship between the water cycle and the

> © 2016 The Author(s). Licensee InTech. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and eproduction in any medium, provided the original work is properly cited.

© 2018 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use,

distribution, and reproduction in any medium, provided the original work is properly cited.

Water and Ecosystem Cycles Mediated by Plant Genetic

**Resources for Food and Agriculture**

Resources for Food and Agriculture

Additional information is available at the end of the chapter

repairing disrupted water and ecosystem cycles.

resources, ecological optimum, agriculture

Additional information is available at the end of the chapter

http://dx.doi.org/10.5772/intechopen.79781

Masatoshi Funabashi

Masatoshi Funabashi

Abstract

1. Introduction

ecosystem.

## **Water and Ecosystem Cycles Mediated by Plant Genetic Resources for Food and Agriculture**

Masatoshi Funabashi

Additional information is available at the end of the chapter

http://dx.doi.org/10.5772/intechopen.79781

#### Abstract

Plant genetic resources for food and agriculture play essential roles in sustainable development and the conservation of global biodiversity. Especially, water cycle and related material circulation are deeply influenced by the loss of plant species diversity and external inputs through agricultural practices. This chapter overviews the water and ecosystem cycles mediated by the ecosystem functions of naturally occurring plant communities and discusses possibilities for the transformation of agriculture into sustainable modality with the primary importance on the recovery of water cycle. The transformation requires an intensive utilization of plant genetic resources in various ways compatible with a multiscale integrated model of water and material cycles based on the processes of ecological succession and evolution. This foresight sheds light on the new importance and utility of plant genetic resources for food and agriculture, in the face of climate uncertainty and in repairing disrupted water and ecosystem cycles.

Keywords: water cycle, material cycles, biodiversity, ecosystem functions, plant genetic resources, ecological optimum, agriculture

#### 1. Introduction

An abundant water cycle supports the ecosystem in the world we live in. Without water filling the earth's surface and flowing back to it, life would not have reached dry land and flourished. Water is the most important substrate for life. The underground water permeating the soil, the rivers flowing through the earth's surface, the lakes creating lush landscapes, and other components of the dynamic water cycle are all supported by the activities within the ecosystem. This chapter looks at the interactive relationship between the water cycle and the ecosystem.

© 2018 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

From the total amount of water cycled across the entire earth, only 0.8% can be used for daily life, such as the underground water and the water in rivers and lakes. About 97% of the earth's water is seawater, and from the remaining 3% freshwater component, 2% is in the form of ice in glaciers in the polar regions. The water that we actually see in our daily life other than on sea is only a portion of the 0.01% water flowing on the ground, out of the 0.8% useable water [1].

This may be a very small number, but this 0.8% component of the water cycle supports the biodiversity on land. Our daily life, and industries such as manufacturing, agriculture, forestry, marine products, and livestock, is established from the various ecosystem services, including domestic water, derived from this component. Water flows in a form that we can use for daily life due to the power of the ecosystem, at the base of which are the plants.

Studying the impacts of agriculture by considering agricultural lands as artificially built ecosystems provides useful insights on the ecosystem and the water cycle. Conventional agricultural practices may be considered as a kind of disruption experiment on the water cycle that is mediated through the ecosystem. In addition, the kind of ecosystem that is created by agriculture is an important consideration in thinking about the future of the water cycle, which supports our daily life.

### 2. Soil functions, water retention, and water purification capacities afforded by the ecosystem

Let us look at how the ecosystem creates a water cycle that supplies water for our daily life. Plants, the primary producers of the ecosystem, play a central role in creating the water cycle for the miniscule 0.8% surface water component. Part of the rainwater supplied to the earth's surface by rainfall goes back to the atmosphere through evaporation and transpiration, and the rest repeatedly penetrates and flows out between the surface and the ground as it flows to the rivers. Within this process, plants—through photosynthesis—create the organic matter that becomes the source of energy for the entire terrestrial ecosystem. Other components of the ecosystem food chain, such as animals and fungi that degrade organic matter, are heterotrophs that depend on the organic matter produced by plants. Photosynthesis is the origin of all the processes on the earth's ecosystem. Thus, plants can be considered as the source of all organic matter on earth, including food and fossil fuel. Photosynthesis, by causing the formation of surface soil, serves as the driving force for the different cycling patterns of useable water, such as underground water, rivers, and lakes.

The electrical properties of surface soil provide clues for understanding the development of surface soil functions. Land, which was originally composed of rocks and minerals, is broken down into various sizes of gravel and eventually into fine clay through long years of erosion and weathering. In particular, since fine pieces of clay carry surface charges, they adsorb the ions needed for plant growth into the ground surface. In the same way that a piece of paper adheres to a sheet of plastic after producing static electricity by rubbing the surface of the plastic sheet, the ions contained in the rainwater are adsorbed by the clay and remain on the ground surface. The growth of plants on the ground and the resulting activities of microorganisms produce various organic substances, which further strengthen the electrical properties of the soil, thereby increasing its water retention capacity and the adsorptive power of microelements. Adsorption and retention of all sorts of substances by the earth's surface enhance the function of purifying the underground water permeating through the ground. As such, the electrical properties of the soil surface provide the key for the synergistic interaction between the production of organic matter and water retention and purification capacities of the soil.

Generally, the topsoil's water retention and purification functions increase proportionally with the diversity of vegetation. This is the reason for the preservation of virgin forests, which are composed of different tree species, as watersheds. Therefore, even under the same climatic conditions, the water cycle components available to living things vary greatly depending on the ecosystem formed on the ground surface layer. Even though the surface water component is only 0.8% of the water cycle for the entire earth, the circulation of this component has a significant impact on the habitat of terrestrial organisms. Imagine what would happen if there was no vegetation on earth, and there was no formation of soil due to photosynthesis. There would be no underground water, rivers, or lakes that would provide a ready supply of water for life. Rainwater would flow straight into the ocean, land would simply release rocks into the sea by erosion, and this world would be nothing but either raging streams of water or dried valleys.

### 3. Merits and demerits of agriculture: decline of usable water cycle components

We need to reevaluate agriculture in consideration of the general role of the ecosystem in soil formation. Usual agricultural practices involve the tillage of land to enhance water retention. This results in a sure but short-term increase of water retention in tilled agricultural lands, sometimes to a level similar to that of forest areas [2]. However, unless tillage is regularly and continuously done, the water retention capacity will not be sustained; that is, without continuous tillage, a hard crust will be formed on the surface to repel rainfall, and the capacity to retain water will eventually be lost. Also, since tillage disturbs the soil ecosystem, it will also eventually destroy the capacity of the topsoil to purify water. In reality, agricultural fertilizers are the biggest pollutants being released to rivers. There are reports of cases wherein, depending on crop species, more than 90% of the nitrogen, phosphate, and potassium—the major components of fertilizers—are not absorbed but become runoff, in agricultural practices that entail tillage and use of fertilizers. This percentage is not for only some farms, but represents the national average in Japan [3].

The emphasis on temporary water retention in conventional agricultural practices clearly does not take into consideration the environmental impact on the ground surface water cycle. Addressing this issue means having to deal with the complexity of the water cycle. First of all, underground water contamination caused by agriculture, unlike industrial and domestic effluent, does not have exact discharge locations, making it difficult to identify testing and sampling points. Also, due to the complex dynamics of underground water penetration, identifying clear causal relationships is not easy, preventing the analysis of the interplay of different farms and timings of fertilization that lead to contamination. If the contamination has accumulated along the river basin, the effects to distant areas, including the marine ecosystem, must also be considered. The complexity of the water cycle widens the extent of the impact, thereby obscuring the location of responsibility for contamination.

The most typical example I witnessed in the field is the runoff of red clay in sugarcane fields in Ishigaki Island. With subsidy from the government, farmers grow sugarcane by tilling land in summer when rainfall is heaviest on 1700 of the 22,900 hectares of the total island area [4]. From an airplane, you can clearly see the red clay flowing in all direction throughout the island and the coral reefs turning reddish brown in color during rain. Fertilizer-containing red clay causes significant changes to the environment of organisms living in the coral reefs, which are said to be responsible for 80% of the biodiversity of marine ecosystems. Recently, there has been an abnormal proliferation of crown-of-thorns starfish around Ishigaki Island, causing damage to the corals. Remains of dead crown-of-thorns starfish are washed up on the beaches, making some areas dangerous to walk barefoot because of their poisonous spines.

Long-time residents of Ishigaki Island claim that they have not seen such occurrences in the past few decades. Although crown-of-thorns starfish is important in creating the diversity of corals, eutrophication due to fertilizer runoff has caused its abnormal proliferation [5].

Thus, although it is clear that agriculture is affecting the environment, it is difficult to make comparisons to identify exact causal relationships and determine the extent of the effects. The selection of factors that must be quantified in order to understand the phenomenon also depends on the purpose and the scale of investigation. Understanding the effect of the coral reef on the ecosystem would require investigating an extensive range of factors that include the fluctuations in marine biodiversity. Likewise, finding correlations between climatic and agricultural factors and isolating individual effects would entail very complicated processes. Therefore, prior to quantifying the complex dynamics of the problem, it would be more effective to qualitatively identify upstream factors and remove them from the targeted systems.

Many years ago, environmental contamination from pesticides, rather than from fertilizers, was the more urgent concern. Pesticides, which have direct toxic effects, more easily became subject to environmental and ethical discussions. At present, most of the pesticides used are highly degradable and do not leave residues in the environment. Even pesticides with low toxicity, however, when used in the long term or in combination, lead to indirect as well as direct effects on the ecosystem—effects that cannot be determined in advance. Likewise, even though fertilizers are in themselves not toxic, they diminish useable water resources once they enter the water cycle, leading to reduction in biodiversity of the water ecosystem, loss in income from fisheries, and damage to the water-related living environment. Also, when using organic fertilizers from livestock farms, there is a need to consider the risk of releasing antibiotics and other chemicals used for animals into the water ecosystem.

Therefore, before the contamination spreads throughout the complex components of the water cycle, the basic surface soil functions must be preserved, and fundamental measures must be implemented in agriculture to prevent the creation of contaminants in the first place. An example of these measures is the incorporation of cover cropping (planting of grasses and legumes in between cropping to prevent soil erosion, enhance the landscape, or suppress the growth of weeds) as part of conventional agriculture practices. Also, since chemical fertilizers and pesticides rely on petroleum resources and rare metals, they cannot be supplied sustainably. Therefore, as long as we do not make use of the natural water retention and purification capacities of the water cycle, which are underpinned by healthy ecosystem functions, the cost for investing on artificial measures would be too high.

The use of genetically modified crops, which have continued to improve in recent years, is gaining wide attention as a means to increase yield while decreasing inputs and environmental burden. This is an effort to shift from the control of environmental factors through the input of material resources to the manipulation of genetic functions. The basic framework of agricultural methods, however, still entails the destruction of soil functions through tillage. In other words, the priority lies in optimizing agricultural productivity under the conventional framework, without consideration of the water cycle functions of the earth's surface afforded by the ecosystem. As such, there are at most only around ten types of environmentally related genes incorporated in genetic modification of crops. This is in stark contrast to the innumerable number of genes that are related to the wide range of ecosystem functions supporting the water cycle and that are expressed by all organisms involved in the formation of surface soil.

It is therefore more important to figure out how to allocate vegetation that supports the core of the water cycle, which involves a numerous number of genes, rather than create a crop that incorporates around ten new genes, in thinking about agriculture that contributes rather than undermines the water cycle. The diversity of the countless genes expressed by plants, animals, and microorganisms in response to the environment is the foundation that supports the water cycle at the genetic level. The interspecific transfer of genes to the surrounding ecosystem through genetically modified crops, however, can have a negative effect on this diversity, and its actual risks are still unknown. In the same way that vigorously introduced species sometimes impair the diversity of indigenous organisms, there is also a risk of diminishing the genetic diversity of endemic species through hybridization with genetically modified crops endowed with dominant functions.

We need to give careful thought on whether it is worth the risk of adversely affecting the diversity of the immensely abundant genetic resources underpinning the water cycle for the sake of optimizing single-crop farming, which is based on the destruction of soil functions. Moreover, even if we can provide proof of whether the transfer of genes from genetically modified crops to the surrounding ecosystem has occurred in the past or not, it is in principle impossible to guarantee that it would not happen in the future.

#### 4. Embankments and flood control

River embankments are an important consideration in thinking about the water cycle of rivers, which are important in agriculture. Rivers overflow by nature, and the riverbanks naturally formed from the flooding, as well as the fertile floodplains around the riverbanks, is in fact ecological structures that naturally create the river's water cycle. The vegetation on the floodplains is what sustains the underground water and functions to store the excess water during flooding, other than being an important source of biodiversity. The fertile floodplains near the rivers are suitable for agriculture and building cities. Due to the resulting advanced economic growth along the rivers, concrete embankments were built along the banks of rivers all throughout Japan to develop the alluvial plains along them. Meanwhile, the growth of the cedars and cypresses that were planted on the mountains in different areas in Japan after World War II has led to the decline of forest floor vegetation, making the mountains more prone to landslides. This has in turn led to the overbuilding of concrete embankments even for the small upstream rivers of mountains.

Cemented riverbanks at a glance seem to protect us from flooding of rivers, but they in fact undermine the diverse water cycle and ecosystem functions of rivers. The water retention capacity and the many other benefits brought about by rivers to the surrounding ecosystem were lost as a result of cementing the passage of water to contain the rivers. Without embankments, the water in rivers freely flows to and from the nearby underground water sources while being filtered through the diverse soil environment. The purification process is compatible with the principle of septic tanks used for the domestic effluent such as from toilets, etc., which are based on physical filtration and adsorption and degradation of organic matter by both aerobic and anaerobic microorganisms. The more diverse the soil environment is, the higher is its capacity to purify water passing through it. The river basin water is purified as it passes through diverse soil types of different physical environments and microbial flora while at the same time enhancing their water-purifying functions.

Cemented riverbanks intercept the free flow of underground water and undermine the inherent purifying function of riverbanks. The Miya River flowing through Ise, Mie Prefecture, is one of the few Class 1 rivers in Japan. According to people living near the river's estuary, before the concrete riverbanks were built, there was no sewage system, there was a large population of residents, and there were some kitchen scraps and garbage floating around. The water, however, was clear, and people were able to dive into the river and catch fish. Presently, however, the population of residents near the estuary has declined, and while a sewage system has been put in place, sludge has built up on the bottom of the water channel and has created a stench. Since disposal of domestic and industrial effluent is restricted, the water quality problem is believed to be caused by fertilizer runoff from the upstream farms and by the loss of purifying capacity of the cemented riverbanks. Also, the decline in the population of eel, which has recently been classified as an endangered species, is believed to be caused, other than by overfishing, by the loss of their habitat due to the building of concrete riverbanks across Japan [6].

Thus, impediments to the natural water cycle result in various trade-offs in ecosystem functions, leading to risks of forfeiting the aggregate benefits afforded by rivers. Since rivers change their courses within the floodplain in response to the water cycle, restricting the flow of rivers at the convenience of human society would only be good for several decades. When we consider the movement of rivers over a hundred-year span, it is possible that the cost of floods that cannot be prevented by the concrete riverbanks and the ecosystem functions lost by building them would exceed the benefits of building concrete embankments. Even the cities and farmlands damaged by the tsunami during the Great East Japan Earthquake were alluvial plains close to the sea level (some were reclaimed areas built lower than the sea level), which basically serve as buffers of the effects of changes in the water cycle.

The Netherlands, Germany, Austria, and other countries have implemented flood control measures that take ecosystem functions into consideration through renaturalization of rivers by removing the embankments and restoring the floodplains. Conventional flood control by building concrete riverbanks has led to the worsening of environmental deterioration and loss of biological resources. Through citizen's movements and policy decisions, consensus is building toward solving these problems by allowing the water cycle of rivers to take its natural course [7].

Large dams built across the USA are approaching the end of their lifespans, and it has been pointed out that they have in fact not fully performed their intended functions in generating power, irrigation, and flood control. Rather, they have adversely affected water quality and the renewal of resources, reduced the underground water in the river basins, and restricted the movement and habitat of wildlife. Because of this, around 850 dams have been demolished in the last 20 years [8]. The dams built around the world are able to hold up to 15% of the total water flowing in all the rivers on earth—an indication of the magnitude of the effect of artificial water reservoirs on the water cycle on the surface of the earth [9].

The renaturalization of rivers is based on the recognition of the environmental deterioration caused by man's efforts to control rivers by artificial means. The concept of renaturalization also includes the extreme approach of completely letting nature take its course by disengaging from all human activity, such as agriculture, in the floodplains. Many aspects of the relationship between ecosystem functions and the water cycle in floodplains still remain unexplained. As the renaturalization of rivers continues to progress, it is therefore necessary to reassess its benefits and shift to a new form of industrial activities that maximize those benefits.

### 5. Agriculture that promotes the ecosystem functions related to the water cycle

Thus far, we have looked at examples of the major effects of both the natural cycling and artificial cycling of water on the ecosystem. The artificial water cycle created by dams and embankments was originally intended to enhance the production of drinking water, energy, and food needed by humans. Since they were built without regard for the effects on the ecosystem and on the natural water cycle, however, they have led to various ills as well. The renaturalization of rivers is a movement to return to the original course of nature upon the realization that the adverse impacts of development are far larger than its benefits. But, is there an example in which the artificial modification of the water cycle has positively enhanced both agricultural productivity and biodiversity?

There is a vast expanse of paddy fields around San Francisco in the USA. The area used to be dry like a desert, but a dam was built to collect water from melted snow from the Sierra Nevada mountains and irrigate the fields, enabling regulation of the water levels to the millimeter level and the cultivation of rice. Applying different concentrations of fertilizers depending on the previous year's harvest enables minimizing fertilizer runoff, and the percolation is blocked by the underlying bedrock. Even though rice paddies are man-made marshlands, they provide a habitat for ducks and various waterfowls and marsh animals. Thus, along with harvesting and other agricultural practices, local volunteers also conduct wildlife conservation activities to protect the young birds and other animals. It is therefore possible to enhance an aspect of biodiversity along with agricultural productivity, even within an artificially created water cycle. Globally Important Agricultural Heritage Systems (GIAHS) represent examples of agriculture that balances productivity and conservation in different countries around the world, wherein moderate disturbance by humans enhances the biodiversity of the environment, such as Satoyama farming (traditional farming in Japan at mountain skirts near the villages) [10, 11].

Would it possible, therefore, to more widely practice agriculture that is based on the relationship between biodiversity and the cycling of water and other resources within the ecosystem? Thus far, agriculture focused too much on continuous production of a particular type of crop, which required a different supply pathway from the natural system for the cycling of materials in the ecosystem, and could not be produced sustainably without the input of external resources. This is very similar to the destruction of floodplains of rivers contained by concrete embankments. The damage from continuous cropping, which is a normal agricultural practice, can be avoided by allowing the succession of vegetation in a natural ecosystem, which is premised on the mixture of a variety of species. In the same way that the natural ecosystem functions of rivers can be restored by enabling flooding to take place, would it be possible to restore the autonomous functions of ecological succession in agriculture?

Let us try to think of an agricultural production system based on the process of topsoil formation, the starting point of which is photosynthesis. This production system should effectively utilize the water cycle, which is nurtured by the process of topsoil formation. Going back to how the cycling of materials has evolved, we see that each material cycles between the various layers comprising the ecosystem. At the beginning, after exposure to rainfall and sunlight, the rocks and minerals were eroded and dissolved into soil solution, where microorganisms started to deposit organic matter, leading to the growth of plants on the first layer of soil formed. Eventually, animals arrived to take up a higher position in the food chain (Figure 1). The current composition of the atmosphere is a result of the total effects of the earth's ecosystem, which has been modified by the evolution of living organisms. Being formed from the lower layers beneath them, the higher layers are more complex, so that the layers can be arranged vertically based on their complexity. We will refer to this arrangement as "axial hierarchy." Figure 2 illustrates how the cycling of materials between each evolution layer takes place. The succession of the ecosystem and the soil forms a network that is intricately entwined with the cycle of materials. By assigning a qualitative complexity score to the soil and ecosystem succession based on the stage of emergence and evolution, and averaging the scores of the layers related to each material cycle, we can arrange them based on the characteristics of emergence and evolution. The resulting order shows a close correlation between the evolution of the ecosystem and the cycling of materials in accordance with the acquired characteristics: In Figure 2 right, the lowest complexity score of material cycle that is Water and Ecosystem Cycles Mediated by Plant Genetic Resources for Food and Agriculture 65 http://dx.doi.org/10.5772/intechopen.79781

Figure 1. Axial hierarchy of emergence and evolution of land ecosystems.

Figure 2. Axial hierarchy of material cycles of land ecosystems. Prepared based on the Figure 18-2 in Ref. [21] by adding the animal layer and leguminous nitrogen fixation. Water movement between animals and transpiration of water from animals were excluded from the relative amount of water.

most involved in the initial process of land ecosystem evolution is the cycle of water, which provides the environment for the emergence of life. Then, on the upper layer followed by the cycle of phosphorus, which is responsible for cell membrane formation, followed by the cycle of minerals, which mediate the signal transduction systems needed for the independent activities of the cell, followed by fixation of nitrogen, by which Archaebacteria carry out nutrient transformation. And, at the top with the highest complexity score of land ecosystem, is the fixation of carbon, which is carried out through photosynthesis, which is in turn responsible for the vegetation covering the entire surface of the earth and for creating the topsoil. Thus, the cycling of materials depicts the evolutionary history entwined within the ecological succession process.

In terms of ecosystem management, if a certain element in the hierarchy is lacking, then a problem occurs. Traditional agriculture tries to solve the problem by supplying the lacking element. However, if the level supplied by the natural cycle is lower than the artificially supplied level, then the system cannot be sustained unless the input is continually made. Conversely, to realize a sustainable culture systems, we need to think about how to change the ecosystem to enable a natural remediation of the material cycle without supplying the lacking element. By fixing the ecosystem layer where the cycle of the lacking element is mostly occurring, it is possible to enhance the cycle of that element within the natural cycle.

For example, to enhance the water cycle, you can plant vegetation with high biomass on finetextured soil to increase the accumulation of organic substances on the topsoil and improve water retention. This increases the volume of water retained by the topsoil for the same amount of rainfall. Also, since the purifying function of the topsoil is dependent on the thickness of the topsoil formed by the vegetation, the capacity to decompose organic substances in the topsoil also increases. Likewise, to increase the amount of phosphorus, minerals, and other microelements, you can plant tree species and vegetation that attract insects and small animals carrying those elements to the field and collect them from surrounding ecosystems. These microelements, other than being supplied through weathering of minerals and through rainfall, are dispersed and retained on land through the activity of fish-eating birds and other animals that collect them from sediments originating from the oceans. Meanwhile, nitrogen, carbon, and other important components of organic matter are accumulated through photosynthetic activities by plants and through the activities of symbiotic microorganisms; therefore, succession of vegetation can be allowed to proceed until the necessary soil formation level is reached.

These measures, however, cannot be expected to immediately satisfy the recommended rates of fertilizer application for single cropping of particular varieties selected by modern agriculture. In contrast, they can enhance the biodiversity of microelements and phytochemicals that are important for exhibiting the ecosystem's functions. It is therefore possible to sustain productivity based on the ecological optimum under mixed growth conditions, which is the basis for primary productivity in natural ecosystems [12].

In order to increase productivity in a highly diverse plant community, there is a need to find the right set of useful plants that grow under the niche of that community rather than practice continuous cultivation of a specific crop. This is the same as improving the cycling of materials by changing their relationships rather than by input of lacking elements. It is possible to balance productivity with the natural ability of the ecosystem to adapt to environmental changes by designing vegetation to enable productivity in a diverse community, in accordance with the cycle of materials and the environment established in the field. Agricultural crops are basically introduced species, wherein despite having more than 30,000 species of agriculturally useful plants, there are only around 120 species actually being cultivated for agriculture. About 90% of all food is derived from only 30 species of plants [13]. Enhancing the water cycle and other ecosystem functions based on biodiversity requires the development and cultivation of underutilized or neglected plant resources in accordance with the ecological succession stage. Synecological farming, or synecoculture, is such an approach to agriculture that emphasizes the management of ecological relationships.

In synecoculture, an extremely wide variety of useful plants are densely cultivated together based on the ecological optimum. This results in a condition wherein the water retention capacity and permeability of the topsoil enhance the water-buffering capacity of the soil while supporting the growth of aboveground vegetation and at the same time enhancing the biodiversity and activity of soil microorganisms [14]. Field experiments conducted in Burkina Faso, sub-Saharan Africa, showed that synecoculture was more efficient in the consumption of water relative to productivity compared to other cultivation methods [15]. These examples indicate that the intensive introduction of diverse genetic resources from useful plants into an agriculture based on the ecological optimum is very effective in improving ecosystem functions, such as the cycle of water and materials.

### 6. Target areas for implementing agriculture that is adaptive to fluctuations in the water cycle

In particular, which places would benefit from an agriculture that emphasizes uninhibited ecological dynamics and the conservation of the water cycle? Governments, NPOs, and scientists from more than 110 countries have submitted an international report stating that agriculture based on large-scale monocropping is not sustainable from the standpoint of environmental burden and fair distribution of food [16]. Also, those who are at higher social risk against the effects of climatic changes are not the developed nations with advanced large-scale agricultural systems, but the small and developing countries in the tropical and subtropical regions [17]. In particular, the increasing expanse of flood-stricken areas in Southeast Asia is at a high risk of being unable to cope with dramatic changes in the water cycle if conventional agriculture is continued, pointing to the urgent need for developing agriculture that leverages the inherent water-buffering capacity of the ecosystem. In China, 200 million small-scale farms are pursuing modernization with support from the government. There is a need, however, to implement measures to improve food production based on the ecological optimum rather than through conventional agricultural practices, both from the standpoint of environmental burden and the available materials and resources in the future [18]. In India, where the Green Revolution has since steadily increased food production and enabled overcoming hunger, restoring the biodiversity and ecosystem services (particularly pollination and purification of water and air) that were lost as a result of the agricultural activities must be addressed [14]. Moreover, African countries undergoing rapid development in recent years must develop self-sustaining agriculture practices based on the characteristics of the ecosystem in each region, in order to combat desertification in arid areas, correct the disparity in wealth, and stabilize their society [15, 19]. To arrest the deforestation of the few remaining tropical rainforests in Indonesia, the Amazon in South America, the Congo Basin, and other susceptible areas, we need to nurture the capacity of local communities to use forest resources sustainably based on the ecological optimum of useful plant resources. We also need to create regulations that favor local economic development and involve stakeholders from a wide range of sectors. These regions will benefit from the rapidly increasing uptake of mobile terminals and other IT devices through the development of databases and tools for understanding relationships with the water cycle and biodiversity primarily pertaining to useful plant resources. These databases and tools will serve as effective infrastructures for underpinning next-generation ecosystem management and food productivity [20].

#### 7. Conclusion

This chapter reviewed the relationship between biodiversity and ecosystem cycles in plant communities with a particular focus on water cycle. A wider introduction of plant genetic resources for food and agriculture into the establishment of novel agricultural practices that make use of ecologically optimum formation of mixed communities is needed to overcome sustainability burdens, cope with the climate change, and recover globally disrupted water and material cycles. Guidelines for the resolution through ecosystem management are explained along with the "axial hierarchy," as a structure traversing ecosystem cycles closely related to the emergence and evolution of land ecosystems.

#### Acknowledgements

This research is supported by Sony Computer Science Laboratories Inc. and the Center of Innovation Program "Global Aqua Innovation Center for Improving Living Standard and Water-sustainability" from the Japan Science and Technology Agency, JST.

#### Conflict of interest

The author declares no conflict of interest.

#### Author details

Masatoshi Funabashi1,2\*


#### References

