**2. Flowering of soybean**

Data for soybean production in two regions are shown in Figure 3 for the period between 1976 and 2012. The production increase in central Brazil made it the largest soybean produc‐

A Comprehensive Survey of International Soybean Research - Genetics, Physiology, Agronomy and Nitrogen

The southern region, which consists of "Rio Grande do Sul", "Paraná", and "Santa Catari‐ na", is now the second biggest producer. The stunning increase in soybean production dur‐ ing this period is similar to the rise of sugar cane during the colonial period and the rise of

The explosive growth of soybean production in Brazil (30 fold increase across a 30-year peri‐ od) has profoundly changed the Brazilian agriculture. It has boosted farming activities; modernization of the transport system; expansion of the agricultural frontier; professionali‐ zation and expansion of the international trade; modification and enrichment of the Brazil‐ ian diet; acceleration of the country'surbanization;and population movement from coastal to

By the 2010/2011 growing season, soybean production had reached the equatorial region of northern Brazil. Thus, a crop that originally was grown only in southern Brazil became well

Data in Figure 4 shows that 82% of production come from the states of "Mato Grosso", "Par‐

However, 13% of soybean production come from the northern state "Tocantins" and the

**Figure 3.** Brazilian soybean production in two regions, in the period between 1976 and 2012. Source: [6].

established in central Brazil and continued to advance into northern Brazil.

er in the country.

Relationships

346

coffee during the Empire era.

the interior areas [1].

aná", "Rio Grande do Sul' and "Goiás".

northeast states "Maranhão", "Piauí" and"Bahia".

#### **2.1. Photoperiod and Photoperiodism**

Soybean culture is sensible to photoperiod and temperature and, due to the great diversity among cultivars, problems of adaptation to certain areas may occur [2]. In environments with constant photoperiods, temperature greatly influences flowering time [8]. There is an inverse relationship between temperature and the average number of days to first flower [9]. Days to first flowering are minor when over night temperatures range from 21 to 27°C. As temperatures fall below this range, first flowering is delayed. Above 27°C, flowering is largely inhibited [10].

The length of a day is known as photoperiod and plant developmental responses (i.e. phe‐ nology) to photoperiod are called photoperiodism [11]. Photoperiod affects not only days to first flowering, but also lengths of subsequent developmental stages. Variations in the day length are determined by latitude and planting date and both affect photoperiod becauseof tilting of the earth's axis. Plants may respond differently to these changes, as they cause modifications on some processes such as seed germination, inhibition of stem elongation, synthesis of chlorophyll and anthocyanin, leaf expansion, flowering and tuberization. The process by which light regulates plant development is called photomorphogenesis [12].

Soybean is strongly influenced by photoperiod so the culture grows and develops according to which photoperiod is subjected. Soybean is classified as a quantitative short-day plant, which means developmental timing is greatly speeded up and reproductive growth en‐ hanced when day length falls below a critical level. This critical level (called the critical pho‐ toperiod) differs with cultivar and maturity group. Soybean responds differently to day length. Differences were observed during the flowering period of soybean when grown on different dates. The discovery of the importance of photoperiod on soybean flowering ena‐ bled the soybean classification as short-day plants [8].

Another important concept is the meaning of critical photoperiod, which is related to the quantity of light hours that can cause flowering. The time interval, in number of days be‐ tween emergence and flowering, is influenced by temperature and photoperiod. There is a limit of the short-day length necessary to induce or to stop flowering. This period is charac‐ terized as critical photoperiod [13]. The length of the critical photoperiod also varies among soybean cultivars [14].

The soybean, classified as a short-day plant, only flowers, or flowers more rapidly, when the number of light hours does not exceed the critical period of the considered cultivar for each 24-hour cycle [15].

When undergoing photoperiodic induction, leaf buds are transformed into flower buds. The development of the flower primordial in the Biloxi cultivar started under short days and the flowers opened after three weeks, showing that there is a period between the received in‐ duction and anthesis [16]. The authors concluded that initiation of floral induction in soy‐ bean occurred with the expansion of the first primary leaves. Further research with Biloxi demonstrated that floral buds were initiated when there was a minimum night length of 10 and a half hours along two or three consecutive photoperiods [17].

When soybean is grown in its adapted area, floral initiation occurs approximately three weeks after germination. Flowering will occur three to five weeks later. Thus, there is a period of approximately three weeks between both developmental stages [18]. Therefore, days to first flower can range from 45 to 50 days depending on the prevailing photoperiod/ temperature and genotype. The minimal period for optimal yield is 45 days from emer‐ gence to first flower [19].

Floral induction occurs during the night. It is determined by the duration of darkness and not the number of light hours. This has been demonstrated by studies in which flower‐ ing occurred as a result of changes in the night length but not in the day length; and by other studies in which interruption of night time by light breaks altered the flowering response [20]. For example, soybean flowered under either short or long days, as long as nights were short [21].

Several researches in soybean characterized influences of photoperiod in the sub period be‐ tween emergence and flowering plants [22-25].

Once soybean ends the juvenile phase and is able to perceive the stimulus, and photoperiod conditions are inductive, the plant enters the inductive phase and vegetative meristems change and start producing floral primordials. After the inductive phase is complete and floral orga‐ nogenesis starts, the plant is in the post-inductive phase until flowering occurs [26].

The sub-period between emergence and when soybean responds to the photoperiod stimu‐ lus is termed as the juvenile phase. Recent research showed that soybean has little sensitivi‐ ty to photoperiod during the juvenile phase [27].

The lengths of such sub-periods are determined by the degree of photoperiod sensitivity of the genotype. Thus, under long days and/or low temperatures, the rate of floral induction and flower development is minor. Developmental rate is important for yield determination, because if the plant develops too rapidly towards first flowering and seed initiation, there will not be enough time to build enough dry matter for optimal yield. Vegetative dry matter accumulation stops at the start of seed filling [26].

### **2.2. Phytochrome**

modifications on some processes such as seed germination, inhibition of stem elongation, synthesis of chlorophyll and anthocyanin, leaf expansion, flowering and tuberization. The process by which light regulates plant development is called photomorphogenesis [12].

A Comprehensive Survey of International Soybean Research - Genetics, Physiology, Agronomy and Nitrogen

Soybean is strongly influenced by photoperiod so the culture grows and develops according to which photoperiod is subjected. Soybean is classified as a quantitative short-day plant, which means developmental timing is greatly speeded up and reproductive growth en‐ hanced when day length falls below a critical level. This critical level (called the critical pho‐ toperiod) differs with cultivar and maturity group. Soybean responds differently to day length. Differences were observed during the flowering period of soybean when grown on different dates. The discovery of the importance of photoperiod on soybean flowering ena‐

Another important concept is the meaning of critical photoperiod, which is related to the quantity of light hours that can cause flowering. The time interval, in number of days be‐ tween emergence and flowering, is influenced by temperature and photoperiod. There is a limit of the short-day length necessary to induce or to stop flowering. This period is charac‐ terized as critical photoperiod [13]. The length of the critical photoperiod also varies among

The soybean, classified as a short-day plant, only flowers, or flowers more rapidly, when the number of light hours does not exceed the critical period of the considered cultivar for each

When undergoing photoperiodic induction, leaf buds are transformed into flower buds. The development of the flower primordial in the Biloxi cultivar started under short days and the flowers opened after three weeks, showing that there is a period between the received in‐ duction and anthesis [16]. The authors concluded that initiation of floral induction in soy‐ bean occurred with the expansion of the first primary leaves. Further research with Biloxi demonstrated that floral buds were initiated when there was a minimum night length of 10

When soybean is grown in its adapted area, floral initiation occurs approximately three weeks after germination. Flowering will occur three to five weeks later. Thus, there is a period of approximately three weeks between both developmental stages [18]. Therefore, days to first flower can range from 45 to 50 days depending on the prevailing photoperiod/ temperature and genotype. The minimal period for optimal yield is 45 days from emer‐

Floral induction occurs during the night. It is determined by the duration of darkness and not the number of light hours. This has been demonstrated by studies in which flower‐ ing occurred as a result of changes in the night length but not in the day length; and by other studies in which interruption of night time by light breaks altered the flowering response [20]. For example, soybean flowered under either short or long days, as long as

Several researches in soybean characterized influences of photoperiod in the sub period be‐

and a half hours along two or three consecutive photoperiods [17].

bled the soybean classification as short-day plants [8].

soybean cultivars [14].

Relationships

348

24-hour cycle [15].

gence to first flower [19].

nights were short [21].

tween emergence and flowering plants [22-25].

Promotion or inhibition of the rate of phenological development in soybean is regulated by the phytochrome pigment in the plant. This has been amply demonstrated by night-break studies in which the effect of a long night (or short day) on promotion of flowering is inhib‐ ited when a light flash is given early in the night period [28]. Period from emergence to first flower is not only controlled by this mechanism, but also by the rate of phenological devel‐ opment for later reproductive periods [14].

Phytochromeis a blue pigment consisting of an apoprotein, which in turn is connected to a tetrapyrrole fitocromobilina, which serves as achromophore. The chromophore is synthesized in the plastid and is the unused portion of the phytochrome protein respon‐ sible for light absorption. The combination of the chromophore with the apoprotein oc‐ curs in the cytoplasm.

The phytochrome is found throughout the plant, but the highest concentration is found in the apical meristem of the stem. This is a plant pigment associated with membranes. The phytochrome molecule has two forms, one more stable and inactive and other more unsta‐ ble and active, working to activate or inactivate reactions, respectively.

Both forms can be transformed into one and another. One form of the phytochrome pigment absorbs far red light (Pfr) at a wavelength of about 730 nm, while the other form of the pig‐ ment (Pr) absorbs light in the red range of about 660 nm (Figure 5).

During the day, plants have both forms, with a predominance of Pfr since normal daylight typically has a ratio of red/far red light of about 1.20. During the night, the Pfr form sponta‐ neously converts into Pr. This reversal is essential for the measurement of time by plants as it determines how phenological developmental rate is affected.

**Figure 5.** Photoisomerization between C and D rings of the chromophore. The absorption of red for Pr, resulting in the change of the ring D of the cis form (inactive) to the trans form (active) characteristic of Pfr. The protein bound to the chromophore is also changed in its shape.

Temperatures during the night affect the rate of this dark reversion of Pfr to Pr [29]. Appli‐ cation of a red flash of light in the night period inhibits the dark reversion of Pfr to Pr and prevents the effect on the developmental rate induced by normal dark reversion of Pfr to Pr.

Research in the late 1980's identified genes in the *Arabidopsis thaliana* plant that are related to the phytochrome encoding. Five phytochrome genes were isolated from this species: PHYA, PHYB, PHYC, PHYD and PHYE that encode the PHYA, PHYB, PHYC, PHYD and PHYE apoproteins. These proteins constitute the chromophore of the phytochrome [30].

In tomato plants (*Lycopersicumesculentum* Mill.) five genes that encode apoproteins were iden‐ tified: PHYA, PHYB1, PHYB2, PHYE and PHYF [31]. When a phytochrome has the PHYA apoprotein, it is called type 1 phytochrome. All others are called type 2 phytochromes.

The difference between the two types is that the first one is accumulated mainly in plants grown in the dark and is easily degraded by light. The mechanisms that contribute to the abundance of the type 1 phytochrome in the dark is that the PHYA gene is preferentially transcribed under these conditions and its expression is inhibited by light [32].

**Figure 6.** A summary of some transformations of phytochrome. Dashed lines indicating dark reversion and destruc‐ tion do not seem to occur with type 2 Pfr molecules [32].

The phytochrome forms Pr and Pfr interconvert as shown in Fig. 5. (type 1 phytochrome). The second type of phytochrome may be more stable under conditions of darkness [32].The mode of action of photoreceptors in the photomorphogenesis process is still unknown [32]. There are two hypothesis:


### **2.3. Gibberellin**

**Figure 5.** Photoisomerization between C and D rings of the chromophore. The absorption of red for Pr, resulting in the change of the ring D of the cis form (inactive) to the trans form (active) characteristic of Pfr. The protein bound to

A Comprehensive Survey of International Soybean Research - Genetics, Physiology, Agronomy and Nitrogen

Temperatures during the night affect the rate of this dark reversion of Pfr to Pr [29]. Appli‐ cation of a red flash of light in the night period inhibits the dark reversion of Pfr to Pr and prevents the effect on the developmental rate induced by normal dark reversion of Pfr to Pr.

Research in the late 1980's identified genes in the *Arabidopsis thaliana* plant that are related to the phytochrome encoding. Five phytochrome genes were isolated from this species: PHYA, PHYB, PHYC, PHYD and PHYE that encode the PHYA, PHYB, PHYC, PHYD and PHYE

In tomato plants (*Lycopersicumesculentum* Mill.) five genes that encode apoproteins were iden‐ tified: PHYA, PHYB1, PHYB2, PHYE and PHYF [31]. When a phytochrome has the PHYA apoprotein, it is called type 1 phytochrome. All others are called type 2 phytochromes.

The difference between the two types is that the first one is accumulated mainly in plants grown in the dark and is easily degraded by light. The mechanisms that contribute to the abundance of the type 1 phytochrome in the dark is that the PHYA gene is preferentially

**Figure 6.** A summary of some transformations of phytochrome. Dashed lines indicating dark reversion and destruc‐

The phytochrome forms Pr and Pfr interconvert as shown in Fig. 5. (type 1 phytochrome). The second type of phytochrome may be more stable under conditions of darkness [32].The

apoproteins. These proteins constitute the chromophore of the phytochrome [30].

transcribed under these conditions and its expression is inhibited by light [32].

the chromophore is also changed in its shape.

Relationships

350

tion do not seem to occur with type 2 Pfr molecules [32].

The conversion of Pfrphytochrome to Pr occurs slowly under absence of light. In this condi‐ tion, the synthesis of the enzyme gibberellin 20 oxidase and 3β-hydroxylase is reduced. They are responsible for turning gibberellin 12 (20 carbons) to gibberellin 1 (19 carbons). Un‐ der longer periods of darkness, the following occurs: low concentration of the far red phyto‐ chrome; reduced synthesis of gibberellin 20 oxidase and 3β-hydroxylase; higher concentration of gibberellin 12 and a lower concentration of gibberellin 1. This low concen‐ tration of gibberellin 1 is responsible for flowering in soybean [33]. The authors described the steps related to Figure 7 as follows:

**Figure 7.** Pathway responsible for the production of the pea plants in GA1 [33].

GAs in pea pericarps (ovaries) are synthesized mainly via the early 13-hydroxylation path‐ way. GA12 is a 13-hydroxylated to GA53; Carbon 20 (noted as 20 in the figure) is sequentially oxidized by a GA 20-oxidase from GA53 to GA44, to GA19, and finally to GA20. GA20 is then oxidized by a 3β-hydroxylase to GA1 (a growth-active GA). Both GA20 and GA1 can be oxi‐ dized by a 2β-hydroxylase to GA29 and GA8, respectively. The latter conversion inactivates GA1. In Figure 8, constructed from previous data [34, 35], an increase occurs in the levels of GA1 gibberellin in spinach plants submitted to long days.

Morphologically, the end of the juvenile period occurs when soybean becomes responsive to photoperiodically-induced reproductive growth. The internal metabolism which leads to plant blooming seems to be influenced by several factors such as concentration of carbohy‐ drates and gibberellin. It is difficult to exactly determine what regulates this stage of plant development [33]. Studies on maize plants indicated that gibberellin-deficient mutants showed a delayed transition from the juvenile to adult stage. This fact may be associated with a long juvenile period. The application of endogenous gibberellin regulated time in this transition phase [36]. Juvenile plants cannot be induced to flower even under appropriate photoperiod. At this time, the buds of the apical meristem do not respond to the floral stim‐ ulus, or the young leaves cannot produce enough stimulus for the induction of floral buds [33]. Research has confirmed the second hypothesis.

**Figure 8.** The fivefolfd increase in GA1 is what causes growth in spinach exposed to an increasing number of long days but before stem elongation starts at about 14 days. After [34]; redrawn from data in [35].

Buds of juvenile *Bryophyllum* species were grafted on to adult plants with flowers and they produced flowers. The author concluded that the meristems were competent to flower, but the young leaves produced insufficient amounts of the floral stimulus [37]. In a work with *Perilla*, a short-day plant, it was shown that the second node of the young leaves produce less floral stimulus, and therefore require more inductive photoperiods to induce flowering, as compared to fully mature leaves [38]. The most recent studies on the flowering control of the *Arabidopsis* plant state that the process is regulated by four separate ways:


GAs in pea pericarps (ovaries) are synthesized mainly via the early 13-hydroxylation path‐ way. GA12 is a 13-hydroxylated to GA53; Carbon 20 (noted as 20 in the figure) is sequentially oxidized by a GA 20-oxidase from GA53 to GA44, to GA19, and finally to GA20. GA20 is then oxidized by a 3β-hydroxylase to GA1 (a growth-active GA). Both GA20 and GA1 can be oxi‐ dized by a 2β-hydroxylase to GA29 and GA8, respectively. The latter conversion inactivates GA1. In Figure 8, constructed from previous data [34, 35], an increase occurs in the levels of

A Comprehensive Survey of International Soybean Research - Genetics, Physiology, Agronomy and Nitrogen

Morphologically, the end of the juvenile period occurs when soybean becomes responsive to photoperiodically-induced reproductive growth. The internal metabolism which leads to plant blooming seems to be influenced by several factors such as concentration of carbohy‐ drates and gibberellin. It is difficult to exactly determine what regulates this stage of plant development [33]. Studies on maize plants indicated that gibberellin-deficient mutants showed a delayed transition from the juvenile to adult stage. This fact may be associated with a long juvenile period. The application of endogenous gibberellin regulated time in this transition phase [36]. Juvenile plants cannot be induced to flower even under appropriate photoperiod. At this time, the buds of the apical meristem do not respond to the floral stim‐ ulus, or the young leaves cannot produce enough stimulus for the induction of floral buds

**Figure 8.** The fivefolfd increase in GA1 is what causes growth in spinach exposed to an increasing number of long

days but before stem elongation starts at about 14 days. After [34]; redrawn from data in [35].

GA1 gibberellin in spinach plants submitted to long days.

Relationships

352

[33]. Research has confirmed the second hypothesis.

The latter three pathways all operate in the shoot apical meristem. The four pathways con‐ verge on a number of floral pathway integrators that together regulate floral initiation [33].

Recently, the T locus was identified which contains the FT gene related to flowering. It is expressed in leaves, encoding products that fit the description of a universal flowering stim‐ ulus. This finding comes against the research carried out for decades which sought that sig‐ nal [39]. More studies are still seeking to define the paths of integration that exist among the different routes.

Figure 9 provides a complete consideration on this subject. This topic briefly addresses the GA pathway, when it operates, and what is known about its integration with the other pathways.

The photoperiodic pathway is located in the leaves and involves the production of a trans‐ missible floral stimulus, the FTprotein [33]. The gene flowering locus T (FT) is a major out‐ put of both the photoperiod and the vernalization pathways controlling the floral transition. FT protein acts at the shoot apex of the plant in concert with a transcription factor, flowering locus D (FD).

In long-day plants (LDPs) such as *Arabidopsis,* the FT protein is produced in the phloem in response to CO (Constans) protein accumulation under long days (LD). It is then translocat‐ ed via sieve tubes to the apical meristem.In short-day plants (SDPs) such as rice, the trans‐ missible floral stimulus, the Hd3a protein (*Hd3a – heading date gene*), accumulates when the repressor protein, Hd1(*Hd1 – heading date gene*), is not produced under short days (SD), and the Hd3a protein is translocated via the phloem to the apical meristem [33].

A major quantitative trait locus (QTL) controlling response to photoperiod, *Hd1*, was iden‐ tified by means of a map-based cloning strategy. High-resolution mapping using 1505 segregants enabled us to define a genomic region of ∼12 kb as a candidate for *Hd1*. Fur‐ ther analysis revealed that the *Hd1* QTL corresponds to a gene that is a homolog of *Con‐ stans* in Arabidopsis.

**Figure 9.** Multiple developmental pathways for floweringin*Arabidopsis:*(a) the photoperiodic (long day) pathway, which operates in the leaves; (b) the convergent autonomous (leaf number)/vernalization (low temperature) path‐ way; (c) the carbohydrate (sucrose) pathway; and (d) the gibberellin pathway. Fonte: [33].

In *Arabidopsis,* FT binds to FD, and the FT/FD protein complex activates the *AP1* (*Apetala1*) and *SOC1* genes (suppressor of over expression of*CO1*), which trigger the *LFY (*Leafy) gene expression. *LFY* and *AP1* then trigger the expression of the floral homeotic genes. The auton‐ omous (leaf number) and vernalization (low temperature) pathways act in the apical meris‐ tem to negatively regulate *FLC-* flowering locus C*,* a negative regulator of *SOC1.* The sucrose and gibberellin pathways, also located in the meristem, promote *SOC1* expression [33].

### **2.4. Juvenile Period - Floral Induction in Soybeans**

Some plants are indifferent to photoperiod, i.e., flowering and other developmental events are independent of photoperiod. In Brazil, this phenomenon was observed in the ''Santa Ma‐ ria'' soybean variety and it was concluded that it was indifferent to day length [40].

Studies with soybean defined four stages of development related to flowering [41]:

Phase I - Juvenile - short days do not induce flowering;

Phase II - Inductive – flowering is induced by a minimum number of short days;

Phase III - Regulation - the number of flowers increases with the continuous conditions of induction and

Phase IV - Post-regulation - there is no effect of day length on flowering.

There is a stage in soybean developmentcalled the juvenile period. Juvenility is the name given to the initial phase of vegetative growth when soybean is not responsive to short-dayinduced reproductive development. Until that period is completed, the plant is not cannot start floral initiation, even if it is grown under short days [42]. A determination of the juvenile period of one genotype can be carried out using the technique described in the literature [43]. A plant that flowers later, even under conditions of short days, has a long juvenile period relative to other soybeans. Such genotypes are described as having the long juve‐ nile character [44].

Considering growth and flowering, it can be observed that each cultivar has a typical re‐ sponse in relation to the sowing date [45]. When sowing is early, there is also early flower‐ ing and lower plant heights in the most photoperiod sensitive cultivars. Research has shown that when the photoperiod is favorable, there is a combination of two or more endogenous hormones in the plant that produces biochemical changes in the meristematic cells of vege‐ tative nodes. These cells begin to multiply and differentiate into flower buds [46]. After the juvenile period, a sequence of two short days sensitize the soybean leaves through phyto‐ chrome [46]. During the day, plants have both forms of phytochrome, with a predominance of Pfr. During the night, the Pfr form converts spontaneously to Pr. This reversal is essential for the measurement of time by plants and for the way they respond to photoperiod.

When cultivars having similar maturity are sown at the same time, they may bloom at differ‐ ent times. Thisis attributed to different juvenile periods [47]. During this period, some meta‐ bolic pathways, which are necessary for flowering initiation, are not triggered.The beginning of the studies concentrated on the phenotypic aspects of flowering, relating the effects and not the causes ofthe observed morphological changes. More complex research opened new per‐ spectives to understand such process. There are two hypothesis for the fact that during the juvenile period, plants are not induced to flower even under inductive photoperiod:

**1.** The buds of the apical meristem are not competent to flowering.

**Figure 9.** Multiple developmental pathways for floweringin*Arabidopsis:*(a) the photoperiodic (long day) pathway, which operates in the leaves; (b) the convergent autonomous (leaf number)/vernalization (low temperature) path‐

A Comprehensive Survey of International Soybean Research - Genetics, Physiology, Agronomy and Nitrogen

Relationships

354

In *Arabidopsis,* FT binds to FD, and the FT/FD protein complex activates the *AP1* (*Apetala1*) and *SOC1* genes (suppressor of over expression of*CO1*), which trigger the *LFY (*Leafy) gene expression. *LFY* and *AP1* then trigger the expression of the floral homeotic genes. The auton‐ omous (leaf number) and vernalization (low temperature) pathways act in the apical meris‐ tem to negatively regulate *FLC-* flowering locus C*,* a negative regulator of *SOC1.* The sucrose and gibberellin pathways, also located in the meristem, promote *SOC1* expression [33].

way; (c) the carbohydrate (sucrose) pathway; and (d) the gibberellin pathway. Fonte: [33].

**2.** The young leaves are still unable to produce enough stimulus for the induction of floral buds [33].

Phenotypic observations reported in many articles have characterizedplant response to pho‐ toperiod. Cultivar ''Doko'' was observed to have a long juvenile period [48], based on a long time to flower under short and long daylengths. Late flowering from several sowings was related to the possible existence of a long juvenile period [49]. The "Doko" cultivar was ob‐ tained from a program of selections which were sowedin summer and winter and has long juvenile period [50].

### **2.5. Genetic Inheritance of Flowering**

Genes affecting flowering response, have been studied in *Pisumsativum* and *Arabidopsis thali‐ ana* [51, 52]. The results show that mutations in these species can change various aspects of the photoperiodic control of flowering. Some of these mutations can eliminate the photo‐ periodic responses, which are responsible for flowering induction. Others may simply slow down or speed up responses to photoperiod [33]. Much of the regulatory systems of flower‐ ing are under either positive or negative control and the presence of mutant plants with changes in photoperiodic responses is very common.

Most mutations result in the loss or alteration of the gene activity. After the mutation, the genes that promoteflowering are changed. Mutations that eliminate plant response to photoperiod can block the production of floral stimulus or may interfere with the ability of the meristem to receive the message [33]. Grafting studies have identified genes in *Pisumsativum* that pro‐ mote or inhibit flowering and control the sensitivity of the apical meristem signals [52]. Most cultivars of soybean, respond to photoperiod as follows: when the number of daylight hours is below the critical photoperiod, there is flowering induction. Only few cultivars have the long juvenile character in which the effect of genes to promote flowering is reduced.

Early studies showed that a long juvenile character in soybean is genetically controlled and can be transferred in a breeding program [53]. Under short days, the authors identified re‐ cessive genes that control the trait. The literature on the subject shows that the long juvenile character is conditioned by recessive genes which can be pleiotropically influenced by other genes in the plant [42, 54-59]. Research conducted under "long-day conditions" indicates that the dominant alleles are responsible for the late cycle: E1/e1 and E2/e2 described by [60], E3/e3 reported by [61], E4/e4 described by [62] and E5/e5 by [63]. In the "short-day condi‐ tions", the opposite occurs [53-55]. Under these conditions, the gene J1/j1 was described [64]. Other studies were conducted to determine the type of inheritance. Research was performed under "conditions of short days" with the genotypes "Hill", "Bragg", "UFV-1", "IAC 73-2736" and "PI 159925" [65]. It was observed that the"long juvenile" characteris controlled by one, two or more recessive genes [3]. These and other studies were fundamental to our understanding of theflowering process of soybean plants grown in locations with different latitudes such as occurs in Brazil.

### **2.6. Long Juvenile Period in Soybean - Practical Application**

The possibility of using plants exhibiting the long juvenile character was the solution found by some soybean breeders to delay flowering in short day conditions [42, 54, 58, 66]. Re‐ search on the adaptation of soybeans to the tropics began at the Agronomic Institute (IAC) and the National Center for Soybean Research, in the 1970s. There were crosses among American cultivars which had the long juvenile character. Several genotypes with this trait were identified and used in breeding programs: "Santa Maria", "PI 159925" and "PI 240664" [67]. Identification of the character was done through research by EMBRAPA where long ju‐ venile genotypes were planted from September 20 to October 10. By this method, genotypes were identified that had a sufficient delay in days to first flower to optimize dry matter ac‐ cumulation and yield [66, 68]. The first cultivars developed and recommended for these areas were "Tropical", "Timbira", "BR-10 (Teresina)" and "BR-11 (Carajás)" [68]. Later the following cultivars were released: "BR-27 (Seridó)", "BR-28 (Cariri)", "Embrapa 9 (Bays)", "Embrapa 30 (CVRD)", "Embrapa 31 (Mina)", "Embrapa 32 (Itaqui)", "Embrapa 33 (Cariri RC)", "Embrapa 34 (Teresina RC)", "Embrapa 63 (Mirador)", "MA/BRS-64 (Parnaíba)", "MA/BRS-65 (Sambaíba)", "MA/BRS-163 (Pati)" and "MA/BRS-164 (Seridó RCH)"

The most commonly used cultivars as sources of the long juvenile character are: "Doko", "Doko RC", "Garimpo RCH", "BR/IAC-21", "UFV-16", "UFV-17", "UFV-18", "CAC-1", "CS 301", "MG/BR-46", "MT/BR-45", "BR-9", "FT-Cristalina", "Cristalina FT-RCH", "Tropical", "BR-10", "BR-11" and "Embrapa-33". They allow for a wider sowing time, planting during the offseason, and planting at low latitudes (short-day conditions) [3]. Currently the soybean crop in Brazil has been attacked by the Asian soybean rust, which leads the country to adopt a control measure called fallowing. In such areas, soybean cannot be planted during the off season. The adopted measure is a protection against the Asian soybean rust which has led the country to adopt a control measure called fallowing. In order to stop the rust, produc‐ tion areas are left vacant for part of the year. Asian soybean rust is a disease caused by *Pha‐ kopsorapachyrhizi* Sydow which caused a loss of two billion dollars to the Brazilian soybean crop in the 2005/2006 harvest.
