Parasitic Plants as Vectors for Pathogens

*Anupam Gogoi, Namrata Baruah, Mandeep Poudel, Ruby Gupta, Geetanjali Baruah and Basanta Kumar Borah*

## **Abstract**

Parasitic plants obtain their nutrition from their hosts. In addition to this direct damage, they cause indirect damage to their hosts by transmitting various plant pathogens. There are some 4,500 species of parasitic plants known; out of them, nearly 60% are root parasites and the rest of them parasitise on the shoot parts. *Orobanchaceae* and *Convolvulaceae* are the two mostly studied families of parasitic plants; and the parasitic plants are the chief mode for transmission of the phytoplasmas. The parasitic plants have various modes of obtaining nutrition; however, the information about the mechanism(s) involved in the pathogen transmission by the parasitic plants is limited. The latest biotechnolgical advances, such as metagenomics and high througput sequencing, carry immense promise in understanding the host-parasitic plant-pathogen association in deeper details; and initiatives have indeed been taken. Nevertheless, compared to the other pests hindering crop productivity, parasitic plants have not yet been able to gain the needed attention of the plant scientists. In this chapter, we review and present some of the latest advances in the area of these important plant pests.

**Keywords:** parasitic plants, pathogen, parasitisim, transmission

#### **1. Introduction**

Parasitic plants, like microbes or pathogens, exploit other host plants for water and nutrients. They display a wide range of parasitic lifestyles, from obligate holoparasitism to facultative hemiparasitism [1]. Parasitic flowering plants comprise of 4,500 species distributed in 280 genera in more than 20 plant families and represent roughly 1% of all angiosperm species [1, 2]. Out of total parasitic plants, 60% are root parasites, and the remaining 40% of the parasitic plants are stem parasites [2]. Several well-known and agriculturally important parasitic plant species belong to the families of *Orobanchaceae* and *Convolvulaceae*. Members of *Orobanchaceae* are root parasites, which includes the genera, *Striga* (witchweeds), *Orobanche* (broomrapes) and *Alectra*. Plant species in these genera can cause significant constraints to crop yield and productivity [3]. Species of *Striga* and *Alectra* pose a serious threat to cereal production in sub-Saharan Africa, India, and Southeast Asia. These includes tropical cereals such as corn (*Zea mays*), sorghum (*Sorghum bicolor*), rice (*Oryza sativa*), and millets, as well as sugarcane (*Saccharum officinarum*) [4]. The related species *Phelipanche* and *Orobanche* are destructive plant parasites for broad-leaved crops grown in North Africa, Europe, the Mediterranean and the Middle East [5].

Besides *Orobanchaceae*, the genera, *Cuscuta* (also known as dodder), from the family, *Convolvulaceae*, are known productivity constraints distributed worldwide. The most agronomically important species of *Cuscuta* are *C. pentagona* and *C. campestris* that attack a broad range of host plants, including vegetables, fruits, ornamentals and woody plants [6].

Like fungi and oomycetes, parasitic plants develop specialised feeding structures called haustoria that establish intimate connections with host cells. A haustorium penetrates the vascular tissue of the host plant, forming a bridge between the parasitic plant and its host. The physiological conduit helps in redirecting resources from the host plant into the parasite [5]. These include movement of water, carbohydrates, nutrients, small molecules (e.g., RNA and proteins) and microbes [7–10]. Recent evidence suggested that the movement of biomolecules is bidirectional, which means exchange may occur from the host plant to the parasite and vice versa [11, 12]. Parasitic plants are reservoirs of various microbial groups belonging to bacteria, fungi, viruses and phytoplasmas [9, 13–15]. They can transmit many economically important plant viruses from infected hosts to healthy host plants. Several dodder plants, particularly, *C. campestris* and *C. subinclusa*, are common species that can transmit a range of plant viruses [16]. Besides dodder, *Phelipanche aegyptiaca* (broomrape) has been shown to acquire both RNA and DNA viruses from infected hosts that represent four distinct genera *Cucumovirus*, *Tobamovirus*, *Potyvirus*, and *Begomovirus* [8]. Parasitic plants can also transmit phytoplasmas, which are phloem-limited pleomorphic bacteria that lack a cell wall. Phytoplasma diseases lead to severe yield losses in vegetables, fruit crops, cereals, oilseeds, and woody and ornamental plants [17, 18]. This chapter provides deep insights into the role of parasitic plants in pathogen transmission, their microbiota composition and diversity. In addition, various ecological lifestyles, and management practices of parasitic plants for sustainable crop production is addressed.

## **2. Various modes of parasitism and nutrition of parasitic plants**

Plant parasitism is a fascinating plant–plant interaction with the acquisition of at least some essential resources from the host plant. Parasitism exerts a strong impact on host growth, allometry, physiology, and reproduction [19]. Parasitic plants can be broadly categorised into two groups based on their modes of nutrition: hemiparasites and holoparasites. The majority of the parasitic plants are hemiparasites, ca. 4100 species [20], which meet most of their photosynthetic assimilates using own photosynthetic machinery and the nutrients and water from their hosts. Three hundred ninety parasitic plant species are holoparasites that lack chlorophyll and, therefore, photosynthetically inept. They rely entirely on their host plants for nutrients and water [20]. Both groups of parasites either connect to the host shoot (shoot parasites, or stem parasites, or aerial parasites) or to the root system of the host (root parasites). Majority of the parasitic angiosperm are root parasites (approximately 60%), while the rest are stem parasite [21], except the genus *Tripodanthus*, which infects both roots and the stem of the host plant [22].

Hemiparasites are predominantly xylem-feeders absorbing water and mineral nutrients from host plants. To ensure rapid intake of xylem solutes, hemiparasites undergo rapid transpiration to import hosts' nutrients via the transpiration stream [23]. In some cases, flux of organic carbon flow from host plant to the hemiparasite in the form of xylem-mobile organic elements [24]. Hemiparasites can be further classified into two types based on their degree of dependency upon the host plant: facultative and obligate. Facultative hemiparasites can survive without a host and do not strictly require a host plant to complete their life cycle. Most studied root

#### *Parasitic Plants as Vectors for Pathogens DOI: http://dx.doi.org/10.5772/intechopen.100187*

hemiparasites are facultative in nature [20]. This includes parasitic plants from the families, *Krameriaceae*, *Olacaceae*, *Opiliaceae*, *Santalaceae* and *Scrophulariaceae* [25]. A facultative hemiparasite may live independent of the host, although suffer reduction in growth and fecundity [26]. In most cases, plant size and reproductive performances are compromised [27]. However, these parasites opportunistically parasitise the available neighbouring plants and exhibit optimum growth. For example, a root hemiparasite, *Pedicularis cephalantha* showed improved performance in the presence of a suitable host, *P. monspeliensis,* where the host was observed to be essential for proper development rather than survival [26]. Likewise, host-attached *Rhinanthus minor*, a xylem-tapping facultative root hemiparasite, showed substantially better growth performance compared to the host-unattached parasite [28].

On the other hand, obligate hemiparasites need host plants for completion of their life cycles as these depend mainly on their hosts for essential resources. This includes stem parasites belonging to the families, *Loranthaceae*, *Lauraceae*, *Misodendraceae* as well as some members of *Convolvulaceae*, *Santalaceae*, *Scrophulariaceae*, and *Viscaceae* [25]*.* Obligate parasites require stimulus from the host, specifically xenognosins, to germinate [1, 24, 29]. For example, germination in dust seeded *Orobanchaceae* such as *Alectra* (yellow witchweed) and *Striga* (witchweed) species is induced by a plant hormone strigolactones [1, 30]. Moreover, some host plants promote a lower rate of parasite germination due to reduced production of germination signals. For instance, the germination of *Striga* seeds in response to the root exudates of *Tripsacum dactyloides*, a wild maize, was significantly lower (ca. 38%) than *Z. mays* root exudates [31]. Holoparasites are achlorophyllous and thus are obligate in nature. The majority of the holoparasites are root parasites, while some species of *Cuscuta* (e.g., *C. europaea*) are stem parasites [32]. Unlike hemiparasites, most of the holoparasites spend much of their lives underground and tend to have a lower transpiration rate [33]. They are predominantly phloem feeder and retain soluble carbon, mineral nutrient, and water from the host [34]. Besides macromolecules, RNA-sequencing and proteomic analysis indicated that holoparasite such as *Cuscuta* species (family, *Convolvulaceae*) could perform bidirectional trafficking of phloem-mobile mRNA [35] and proteins [36] between widely divergent species and regulate host gene expression [12]. As the phloem is living tissue, for parasitism, the parasite thus obliges to have biochemical compatibility with its host [37]. Consequently, phloem-feeding holoparasites have complex haustorial structures and are more host-specific than hemiparasites [27, 38]. Apart from their complex haustoria and host preference, phloem-feeding holoparasites have a distinctly lower Ca:K (Calcium:Potasium) ratio because calcium is usually present in very low concentrations in the phloem than in xylem fluid [39]. Phloemfeeding holoparasites also retain features of their xylem-feeding ancestry. However, the xylem bridge form between parasites and their host plants is functionally inactive [40]. On the other hand, some holoparasites show a xylem-only feeding strategy, such as the genera *Lathraea* and *Boschniakia* that acquire host nutrients exclusively through xylem [41]. It shows that all parasites have the universal ability to acquire resources from the host xylem.

Parasitic plants have a broad host range and attack several co-occurring species, often simultaneously. Host range of parasitic plants is a function of the parasites' feeding mechanisms (xylem- or phloem-feeder), distinct events of the evolutionary history of the species, and the biochemical compatibility with the host cells [40]. However, host specificity is largely determined by the extent of reliance on the host plant and depends on the ability of the haustoria to functionally establish after invading the host. The most common potential hosts are from *Asteraceae*, *Cyperaceae*, *Fabaceae*, *Labiatae*, *Poaceae* and *Rosaceae* families [42, 43]. In general,

facultative parasites, specially root hemiparasites, have a broad host range, whereas obligate/shoot parasites tend to be more host-specific [44]. Conversely, holoparasites have a narrow host range compared to hemiparasites due to their greater reliance on host plants. In plant parasitism, host specificity is an exception rather than a rule. A notable exception is a root-parasite *Epifagus virginiana* (beech-drops) which strictly parasitise *Fagus grandifolia* (American beech) [23]. Among shoot parasites, host specificity is particularly seen in mistletoes, for e.g., *Arceuthobium minutissimum* (Himalayan dwarf mistletoe), which only parasitises *Pinus griffithii* (Himalayan blue pine) and *Phoradendrons cabberimum* (Mexican mistletoe) that grow only on other mistletoes [21, 23]. Some species within a genus are found to be in the range of generalist to specialist. For example, among 45 species of the genus, *Arceuthobium* (family: *Viscaceae*), *A. apachecum* parasitise a single host (*Pinus strobiformis*), whereas another parasite, *A. globosum* spp*. Grandicaule*, parasitise 12 different host species [44]. Likewise, tropical rainforest mistletoe *Dendrophthoe falcata* (family: *Loranthaceae*) is known to have at least 343 different host species [20]. Despite their wide host range, parasitic plants prefer host that has readily accessible vascular systems, high nitrogen content (e.g., legumes), lower defence mechanisms and host that provide resources for a longer period (e.g., deep-rooted woody perennials) [19].

### **3. Transmission of various pathogens by parasitic plants**

Plant virus and phytoplasma diseases are major threats to modern agriculture and their management can be quite challenging. Different strategies have been developed to reduce the transmission of these pathogens. It is crucial to understand the various sources of contamination or inoculum during cultural practices to restrict the entry and thereby transmission of viruses in fields [45].

For the parasitic infection to initiate, it is important to understand the aetiology behind the transmission process. For infection in the above ground parts of the host, for instances, *Cuscuta* or *Viscum* species, it is mostly coincidental and occurs mainly through dissemination of seeds by wind, rain, or biotic causes [46]. Conversely, the process of infection is different for obligate root parasites, which depends on factors like presence of stimulants, grouped under strigolactones exuding from the host root surfaces instigating the germination of parasitic seeds. The seeds of obligate parasites like *Orobanche, Phelipanche* and *Striga* are also known to lay dormant without the presence of appropriate hosts in soil for years, whereas for some others, germination without a host eventually leads to their death [5]. Upon germination, the radicle tends to sense the host roots in lieu of chemotaxis such as in *Striga* [47, 48]*.* An example is shown by a time-lapse video of *S. hermonthica* radicle bending towards the host root while it elongates [49]. However, a chemotrophic growth may not be always true in case of some root parasites such as *Orobanche*, where the growth of parasite root towards host occurs without any known factors and only by chance, provided the process of germination take place in close contact to the host plants. One of the essential steps of host-parasitic infection involves the localisation of the hosts, after which their attachment involving the formation of haustoria plays a crucial role in dissemination of viruses and phytoplasma from the infected host to the parasite and thereby initiating the transmission of plant viruses.

The connection between host and the parasite is established with the development of 'prehaustoria' starting from the differentiation of a secondary meristematic tissue from epidermal and parenchymatous tissues of the parasite. Substances, such as pectins, facilitate the adherence and polysaccharides exuded by the prehaustoria and drives the host to produce factors for attachment and penetration [46, 50, 51].

#### **Figure 1.**

*Schematic representation of parasitic plant-host interaction and pathogen transmission. Bidirectional movement of biomolecules such as water, carbohydrate (e.g., sucrose), nutrients (e.g., phosphorus and nitrogen) and nucleic acids (mRNAs and small RNAs), as well as microbes, may occur through physiological conduit form by the haustorium of the parasite with the conductive tissues (xylem and phloem) of the host plant. Many plant viruses and phytoplasmas are acquired and transmitted by parasitic plants from an infected host to healthy host plants. The figure was created using bioRender.com*

After the process of penetration through a fissure in the host stem, the haustoria invades the epidermal and hypodermal tissue to develop inside the vascular bundle [46]. While growing towards the xylem and the phloem tissues, they develop hyphal structures, similar to finger-like projections, also known as 'absorbing hyphae', which behaves like sieve element or transfer conduits for flow of nutrients between parasite and host [5, 38, 52, 53]. These multicellular haustoria functions with the aid of chemicals, also known as haustoria-inducing factors and some tactile cues [54]. In such an interaction, it has been shown that in transgenic tobacco plants parasitised by *Cuscuta*, there has been wide exchange of molecules through the phloem of tobacco plants until the developing leaf primordia [53]. During such passage of resources between the parasites and the hosts, several fluids including proteins and phloem-mobile RNAs are exchanged, which contributes in transmission of virus and phytoplasmas from infected hosts to healthy plants [11, 35]. A detail schematic representation of host-parasitic plant interactions and exchange of biomolecules, microbes and pathogens between host plant and the parasite is shown in **Figure 1**. The reports from various translocation experiments, specially one using *Cuscuta* bridge between with carbon labelled compounds and *Potato Virus Y* in Pelargonium showed symplastic exchange of solutes between the parasitic species and their corresponding hosts [55].
