Plant-Microbe Interactions: A Comprehensive Review E-Book
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- Herausgeber: Bentham Science Publishers
- Kategorie: Wissenschaft und neue Technologien
- Sprache: Englisch
Plant-Microbe Interactions: A Comprehensive Review provides an in-depth analysis of the dynamic relationships between plants and their associated microbes, highlighting beneficial and harmful interactions. The book emphasizes the role of plant growth-promoting microorganisms (PGPMs) and biocontrol agents, covering nutrient acquisition, nitrogen fixation, and plant stress management. It also examines harmful microbes responsible for pathogenesis and biotic stress, offering insights into their ecological and molecular mechanisms.
The book examines microbiomes in both the rhizosphere and phyllosphere, the role of artificial neural networks in studying these interactions, and biotechnological advancements in managing plant pathogens. It brings together cutting-edge research on crop health, sustainable agriculture, and biotechnological innovations, offering comprehensive insights and practical solutions.
Key Features:
- Explores plant-microbe interactions in various environments.
- Details biotechnological applications in plant health management.
- Discusses microbial roles in nutrient bioavailability and stress tolerance.
- Highlights recent advances in pathogen management and crop improvement.
Readership:
Undergraduate and graduate students, researchers, biotechnologists, agronomists, and industry professionals in plant sciences and agriculture.
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Seitenzahl: 458
Veröffentlichungsjahr: 2025
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FOREWORD
Plants, being sessile organisms, are constantly exposed to the infection and disease caused by different microbial pathogens, including bacteria and fungi. The resistance of a plant to a pathogen attack depends on its efficiency in the elicitation of defense molecules like phytoalexins, salicylic acid, jasmonic acid, etc., as well as on the activation of diverse signaling pathways and induction in resistance (R) and pathogenesis-related (PR) genes, altogether triggering plant immunity. However, certain infections caused by microbes are beneficial in nature as well, especially the legume-Rhizobium interaction that facilitates symbiotic nitrogen fixation via nodule formation, or the microbiome association in the rhizosphere region that allows stress tolerance, phytoremediation of heavy metals in soil or stimulates nutrient absorption in nutrient-depleted soil. Hence, plant-microbe association is a double-edged sword, having both detrimental and beneficial consequences. It is therefore crucial to understand this association by identifying and characterizing the biochemical and molecular pathways, using high throughput genomics, proteomics, metabolomics, and genetic engineering techniques. In this regard, this book titled, “Plant-Microbe Interactions: A Comprehensive Review” encompasses quite an exhaustive coverage of important topics, supported by contemporary literature.
The chapters include various facets of co-evolutionary dynamics of plant-microbe interaction, understanding the fungal and viral interactions from a broader perspective, and assuming case studies with particular plant species. Emphasis has been given to the association of nitrogen-fixing bacteria and the biotechnological perspective of legume-pathogen interaction. The inclusion of chapters on rhizosphere and phyllosphere microbiome in the context of stress resistance and increased nutrient acquisition also appears justified, since a lot of research is currently going on in these areas. Researchers working in the field of salt tolerance would benefit from the chapter on halotolerant plant growth-promoting rhizobacteria. The chapter on understanding plant-microbe interaction, based on artificial neural networks is also unique. The chapters presented in this book will collectively address the critical need to understand plant-microbe interactions for the benefit of both the plant community as well as the environment.
I am delighted that this edited volume “Plant-Microbe Interactions: A Comprehensive Review” is finally being published. The chapters are elaborately written by established and active scientists and researchers, working in the concerned area.
Finally, I congratulate the editor for making sincereefforts to unravel this illustrious volume, and I am sure that this book will highly cater to the needs of all researchers, students, and academicians, working in the relevant field.
PREFACE
The plants are constantly interacting with diverse microbial communities in the environments. The constant co-evolution of microbes with plants not only shapes the ecological balance but also determines plants' fitness in a particular environmental condition. The plant-microbe interaction has always been an interesting field of study to decipher unsolved puzzles in these intriguing relationships. Such interactions are of two types, beneficial and harmful interaction. The harmful interaction determines pathogenesis and biotic stress in plants. The beneficial interactions, on the other hand, help plants in nutrient acquisition, nitrogen fixation, and biological control systems against diverse pathogen groups. Although, many studies have been reported demonstrating, biotic stress and beneficial microbes act as plant growth-promoting microorganisms (PGPM) or biological control agents. These two interactions were always studied separately, but in nature both harmful and beneficial microbes interact with the plants synergistically. The in-depth knowledge about the entire interacting microbiome community with plants is necessary to describe this interaction more efficiently. At the same time, knowledge of this balanced interaction would also be useful for future biotechnological and agronomic applications. Recently, many pieces of research have focused on decrypting phyllosphere and rhizosphere microbial communities associated with economically important crop plants to analyze pathovar, core microbiome, and PGPMs. In this view, the present book has been designed to comprehensively accrue contemporary scientific knowledge encompassing all types of plant-microbe interaction for knowledge updation as well as for future agro-biotechnological applications.
In summary, the book is believed to advance our knowledge in the field of plant-microbe interaction, inform practical applications, and contribute to sustainable agriculture, ecosystem conservation, and biotechnological innovations. It addresses the critical need to understand these interactions for the benefit of both plants and the environment.
I would like to thank all the contributing authors for sharing their experiences and enriching the book with their valuable research findings.
My sincere thanks and gratitude are also extended to all the editorial and managerial team of Bentham Science Publishers for their continuous support.
List of Contributors
Co-Evolutionary Dynamics of Plant-Microbe Interaction; A Comprehensive Outlook
Sumanti Gupta1,*Abstract
The co-evolution of plants and their associated diverse microorganisms has been a field of wide scientific research since the past. However, the ecological relevance of such co-evolution has recently been realized. According to the theories of evolution, ‘survival of the fittest’ has been an age-old fundamental concept, where every organism modifies itself to adapt to its changing environment while sustaining its vital processes. Understanding the interactions at the molecular level between the stationary plants and their diverse interacting partners has not only helped in deciphering the basis of evolution but also provided a better outlook towards the multidimensional interactions between the organisms of the plant microbiome. Ideally plant ‘holobiont’ comprises the host and all microbial partners of its different locations such as the rhizosphere, endosphere, and phyllosphere. The behavioral patterns of the microbes with their hosts located at different zones designate them as symbionts, commensals, and/or pathogens. Each type of relationship has its basis of establishment and evolution. The present study aims to explain the basis of the evolution of plant-microbe interaction ranging from symbiosis to parasitism and understanding its evolutionary dynamics from an ecological perspective. Besides, the study shall also explain the role of microbiome in plant-microbe interaction and its ecological significance when subjected to climatic undulations. Overall, the study aims to put forth a comprehensive outlook on the understanding of ecology-driven evolutionary changes of plant-microbe interaction and its relevance in the present age of climate change.
INTRODUCTION
The origin of land plants dates back to 420 million years ago during the period of late Silurian, while the origin of microbes is reported to have occurred much ear-
lier around 3.4 billion years ago [1, 2]. Timeline analyses have shown that the diversification and establishment of plants on land have taken place when the microbial world had already been well settled on Earth. Thus, under the profound ancestral influence of microbial communities how the plants originated, established themselves, and functioned as one of the pivotal entities of almost all ecosystems on Earth, is undoubtedly an intriguing question of evolutionary biology [3]. Plants are not only termed as the food producers of the biotic world but also referred to as niche providers that provide shelter to numerous micro and mega organisms of diverse structures, functions, and behavioral patterns [4, 5]. The history of the origin of photosynthesis however dates back to 1967 when scientist LynnMarguilis (then Lynn Sagan) in her article ‘On the Origin of Mitosing Cells’, published in the Journal of Theoretical Biology hypothesized the origin of solar energy trapping organelle ‘the Chloroplast’. Chloroplast originated when a non-photosynthesizing bacterium engulfed a photosynthesizing cyanobacterium through the unique process called ‘endosymbiosis’. The same process also gave rise to the oxygen-generating organelle ‘the mitochondria’ when an aerobic prokaryotic (possibly alpha-proteobacteria) bacterium was engulfed by a heterotrophic anaerobe. Lynn also suggested that the eukaryotic flagellum (named undulipodium) and the mitotic apparatus were formed from a spirochaete-like organism by endosymbiosis [6]. Increasing phylogenomic evidence has, however, suggested that the present-day distribution of photosynthetic machinery within six phyla, namely 1) cyanobacteria or blue-green algae,2) proteobacteria of purple bacteria, 3) green sulfur bacteria, 4) heliobacteria or firmicutes, 5) green non-sulfur bacteria and 6) acidobacteria have taken place by horizontal gene transfer (HGT) through independent phylogenetic lineages, which makes the evolutionary tree of photosynthetic very complex. All the above-mentioned bacteria were phototrophic except proteobacteria [7]. Although photosynthesis is known as a well-concerted metabolic process its various subsystems such as photosynthetic pigments, light-harvesting antenna systems (LH), reaction centers (RCs), electron transport, and carbon fixation pathways are believed to have originated via diverse evolutionary trails [8].
Besides photosynthesis, plants are known for their distinctive ability to provide habitation to diverse groups of organisms. Plants are believed to have probably acquired the said property because of their sessile nature, which occurred with the migration, settlement, and colonization of plants from aquatic environments to land locations. The aquatic paraphyletic group of green algae belonging to Charophyta with the order Zygnematales is reported to be the nearest ancestor of land plants [9]. Zygnematales members were marked for the absence of motile sperms which the remaining Charophytes possessed. Such gradual retraction of flagella leading to the cessation of motility possibly was a transition where mobile lower groups of plants started adapting to land habitats [3]. Interestingly, the origin of land plants from the algal ancestral lineage showed exciting illustrations of bacterial-algal interactions that put possible endorsements to the fact that biotic interactions not only shaped the algal evolution but also had a signature role in the colonization of land plants [10]. Phylogenomic studies suggested Zygnemataceae family members Spirogloea muscicola gen. nov. and Mesotaenium endlicherianum to be the closest members of earliest diverging embryophytes and bryophytes; all of which shared similar sub aerial/terrestrial traits. Genetic analyses further indicated the presence of significant genes that controlled biotic and abiotic stress resilience properties (desiccation tolerance) both in Zygnematacean members as well as early land colonizing embryophytes and bryophytes. These genes were found to have originated from soil bacteria by HGT [11]. Hence, it remains clear that the event of terrestrialization of plants, considered one of the most significant phenomenons of the evolution of life on Earth, was predominantly controlled by the primeval residents of Earth, the microorganisms.
Thus, once settled, plants gradually acquired roots and vascular systems giving rise to different classes of plants that adapted to the land habitats. On the other hand, the rooted nature made the plants sessile and exposed them to diverse groups of interacting partners with varied behavioral patterns. Although remarkable developments have taken place over the past few decades in establishing the modes and mechanisms of plant-microbe interaction, even then research, long-standing discussions, and debates continue to argue about why and when a plant and microbe/s enter into communication. However, high throughput experimental studies have established that signal-mediated sensory manipulation of both interacting partners termed the ‘Coercion’ property is the main guiding force behind the initiation of communication [12]. Previous research on coercion suggested having two modes of stabilized coercive communication where microbial coercion means manipulating plant phytohormones while plant coercion suggests maneuvering quorum sensing infochemical of microbes [12]. Amongst several interacting partners, plants coexist with some microbes that facilitate their growth and development and are called symbionts, some remain as commensals with no advantage to the host plant, while a handful modify themselves and compete with the host plants for nutrition and space and get transformed into pathogens [13]. Besides some other microorganisms which surround the host plant may have no direct influence on the host performance under a particular spatial and temporal scale, but may reprogram themselves to hold direct or indirect influence on the host plant under changing climatic conditions. All the above microbes with their differential behavioral patterns are referred to as the ‘plant microbiome’ where all the organisms individually serve as a ‘metaorganism’ [14, 15]. The entire plant microbiome is reported to have an impact on shaping the ecological evolutionary trajectories with ‘plant holobiont’ (the host and its associated microorganisms that directly influence plant growth and immunity) being referred to as the ‘second genome’ and primary contributor of ecological stability and sustainability [15, 16]. Similarly, the death and decomposition of a single microbe and/or a microbial population of plant holobiont bring about an entire shift in the biodiversity thus altering the functional outcome of a given ecosystem. Such a shift in structure and function at the ecological scale by a single or a group of organisms is referred to as ‘Dysbiosis’, a concept which is recently been perceived as an amendment to understanding the plant-microbe interactomics and its evolution [15].
Recent advancements in technological tools and analytical methods have made remarkable additions to the understanding of plant-microbe interaction beyond the one-to-one interaction models. Nevertheless, understanding the ecological relevance of such intricate multidimensional interconnections and intra-communications is still in its infancy. Thus, the present study aims to revisit the well-explained concepts of plant-microbe interaction and explain the basis of its evolution of mutualism and competition leading to pathogenesis. Besides, the study shall also attempt to explain the alteration of the microbiome with respect to unpredicted climatic undulations and its ecological significance on plant-microbe interaction. Thus taken together, the study is expected to put forth an inclusive outlook on understanding the evolution of plant-microbe interaction and its relevance with the present age of climate change.
PLANTS SERVE AS HOSTS FOR DIVERSE MICROORGANISMS OF DIVERSE BEHAVIORAL PATTERNS
Below Ground Interacting Partners
Plants being sessile house many organisms of varied structural and behavioral patterns. Amongst many parts, the belowground roots provide a dynamic environment that is exploited by many organisms making the underground microbiome a rich biodiverse hotspot. Roots are believed to serve as a highly specialized and sophisticated interface between the host plant and its surrounding microbial zone. The interface is again sub-compartmentalized into segments named the rhizosphere, endosphere, and exosphere, each of which harbors specific organisms that indulge in intricate inter and intra-zonal signal exchanges, which not only facilitate mutualisms between host plants and interacting microbes but also shield host plants from pathogen mediated damages [17, 18]. The rhizosphere is referred to as a highly specialized zone surrounding the root periphery. It is known to harbor different microbes such as bacteria, fungi, oomycetes, nematodes, etc. Additionally, the root surface tissue facing the exterior called the rhizoplane (also exosphere) is also known to play a significant role in controlling plant-microbe interaction and enhancing plant fitness [19]. The rhizosphere serves as an additional barrier from the pathogenic intruders of the host, which acts as a well-habitable locale for symbiotic organisms. This zone is known to possess a complex array of energy-rich carbon compounds that on one hand support the growth and metabolism of mutualists while on the other hand, contain different antimicrobials released as root exudates that prevent the invasion of harmful pathogens. The beneficial plant growth-promoting rhizobacteria (PGPR) are known to produce rhizodeposits that promote plant health and immune responses. Thus, the root cell exudates, rhizodeposits, and the signal transductions taking place at the interface of root border cells are known to modulate the performance of the host as well as maintain the uniformity and stability of its root holobiont [20]. However, some interacting partners may remain as commensals themselves being benefitted but imparting no supportive services to its host plants. The basis of belowground commensalism and its persistence which is thought to be under special and temporal influence is ill-studied [21]. However, some microbes of the rhizosphere are often reported to undergo transformational reprogramming and become pathogenic competitors of their hosts, thus competing for nutrition and space. Besides, other soil organisms comprising plant microbiome but not behaving as part of plant holobiont also indirectly contribute to plant performance by influencing the inter-signal communication with the microbiota of plant holobiont. Thus the demarcation of soil microbiome, plant microbiome, and plant holobiont appears to be quite blurred belowground and readily gets altered with the slightest shift in the predisposing factors. Root endospheric organisms are also known to contribute largely to the host physiology and metabolism. These endospheric organisms are capable of crossing the barrier of the rhizosphere, and root epidermis and colonize at the cortical cells, stele, and vascular cylinder of the root interior [22]. The endophytic organisms comprise bacterial and fungal members, which are known to aid the host by controlling its nitrogen cycling, internal phosphate transportation, immune responses, and antibiotic production which all together ward off harmful pathogens and uphold plant fitness [23].
Above-ground Interacting Partners
Similar to belowground microbiome, aboveground microbiome is also considered to be an abundant biodiverse zone. This aerial part is referred to as the phyllosphere with its microbiome termed as ‘phyllobiome’, comprising the other important part of plant holobiont. This part of the host is also known to provide a niche to a large group of microorganisms such as bacteria, fungi, viruses, actinomycetes, cyanobacteria, etc. Phyllospheric microbes are also reported to occupy external regions as epiphytes and interior zones as endophytes. These zonal microbes not only support plant growth and immunity but also equip the host with adequate resilience mechanisms that help them adjust and adapt accordingly during abrupt climatic undulations as well as during anthropogenic disturbances [42]. Alternatively, host plants are also known to reorient their metabolic output to support the growth and multiplication of beneficial microbes and endow them with adequate reserves so that they can not only outnumber harmful pathogens but also maintain active surveillance against their ingress [43]. This is done by the secretion of several chemical stimuli that conditionally recruit beneficial organisms in large populations and outnumber pathogens, a phenomenon called ‘cry for help’, which although well studied in belowground microbiomes lacks adequate reports in above-ground microbiomes [44]. Table 1 enlists some predominant microbes of the phyllosphere.
THE WHY AND HOW OF PLANT-MICROBE INTERACTION; UNDERSTANDING THE MOLECULAR DYNAMICS AND ITS EVOLUTION
The Molecular Evolution of Symbiosis
Previous experimental studies have well established the fact that terrestrialization of land plants has taken place following endosymbiosis that gave rise to appropriate organelle such as the chloroplast and mitochondria, which helped the plants in their basic survival and sustenance under phototrophic and aerobic land conditions [45]. Hence host-microbial symbiosis is undeniably an early event to have taken place in the evolutionary pathway of plant-microbe interaction that not only aided the water-to-land relocation but also structured the life of land on Earth. These newly migrated land hosts somehow became compelled to provide adequate accommodation and accessory requisites to these groups of symbionts, which in turn extended help in terms of providing growth promotion and resistance against pathogens to their hosts. Intracellular symbiosis relied on conserved genetic modules that the hosts obtained from lineage-specific supplements (reported as modified defense-related genes), while intercellular symbiosis evolved as a result of convergent genetic supplements [46, 47]. Similarities in gene expression patterns during symbiosis and/or pathogenesis of non-vascular plants such as Marchantia and Lycopodium and model angiosperms such as Arabidopsis, Medicago, and Lotus suggested that the same set of conserved genes exhibited dual roles that were either similar or mutually opposite in promoting symbiosis or pathogenesis. However, symbiosis and/or pathogenesis probably depended on specific temporal and spatial conditions and related predisposing factors [48]. For example, Medicago truncatula genes such as DMI1, LIN, LYK3, NFP, NSP1, and CERK1 showed an enhanced expression that positively regulated arbuscular mycorrhizal (AM) symbiosis but negatively influenced the entry of pathogenic filamentous fungi and oomycetean members. Conversely, mutations of genes such as RAD1 or RAM2 or RNAi-mediated silencing of ROP9 contributed to gene regulation in a similar fashion during both AM symbiosis and oomycetes infection [49]. Such examples suggest that homologous and frequently orthologous genes belonging to specific protein families govern the process of symbiosis and/or pathogenesis under specific conditions and in specific plant lineages [48]. The history of evolution of symbiosis suggests that four types of symbiotic relations occurred of which symbiotic interaction between AM fungi and bryophytes originated approximately 480 million years ago [50]. Following this ectomycorrhizal fungal (EM) association between angiosperms and EMF took place apparently 220 million years ago [50]. The origin of plant-nodulating bacterial interaction probably occurred when AMF and EMF-associated plants faced nitrogen starvation which took place about 100 million years ago [51]. The association of plants and Frankia (actinobacteria) also occurred sometime around 100 million years ago.
The past research works have mentioned that AMF interaction took place initially with bryophytes, which lacked proper roots and hence had limitations regarding nutrient acquisition. On the other hand, the AMFs which belonged to class Glomeromycota, a small group of fungi that were known to behave as obligate endosymbionts, possessed the ability to penetrate the plant cell wall, induce profuse branching in planta and form arbuscules inside root cortex [50]. Molecular analyses suggested that plant-induced signaling molecules such as strigolactones and flavanoids are perceived by an unknown receptor of AMF. AMF then undergoes modifications that promote spore germination, branching, and secretion of reciprocal symbiotic signal, which altogether help in the process of colonizing the host plants. AMF symbiotic signal cocktails comprise Myc factors, effector proteins, short-chain chitin oligosaccharides (COs), and lipo-chitin oligosaccharides (LCOs) [52]. Reception of AMF symbiotic signals is reported to activate potassium channel protein DMI1 located at the nuclear membrane that in turn triggers calcium signaling cascades that are further linked to downstream activation of conserved ‘common symbiosis signaling pathway’(CSSP) [53]. The calcium undulations in CSSP are sensed by calcium/calmodulin-dependent protein kinases (CaCMK), which induce the expression of the GRAS transcription factor [54]. The CSSP is known to suppress host innate immune signals and facilitate the attachment and entry of hypha into root surface and cortical cells respectively that finally leads to the formation of arbuscules. At this stage, the role of CSSP ceases and an optional pathway that caters to nutrient acquisition of symbiont becomes operational [53]. Nutrient acquisition is considered a hallmark for the establishment of symbiosis, which is achieved by the bidirectional nutrient exchange between AMF and host. The AMF provides soil-acquired phosphate and nitrogen to its host in exchange for the sugars and lipids [55]. Apart from AMF, ectomycorrhizal fungi (EMF) are known to help the host in carbon confiscation from the soil, nutrient mobilization within the host interior, preventing pathogenic invasion, etc. EMF is reported to release effector protein and aquaporins after contact with the host root surface. Following this, profuse hyphal branching takes place leading to the formation of ‘Hartig Net’ that is covered with a thick layered outer mantle [56]
Reports suggested that plant-rhizobial interaction originated much later as compared to AMF/EMF-plant interaction. Rhizobium is known to produce nitrogen-fixing nodules in approximately 70% leguminous plants and only one non-leguminous plant named Parasponia sp [57, 58]. The evolution of plant rhizobia is diverged into two schools of thought. The first one presumes the origin to be from multiple lineages, which gave rise to the nodulation event distantly in legumes and non-legumes [59, 60]. However, the more recent hypothesis suggests nodulation have evolved from a single angiospermic lineage of rosids clade 1, which was already in a relationship with an AMF [51]. However, the occurrence of consistent root-nodule symbiosis was achieved by many loss and regain back events which probably made the association highly host-specific [61]. On the other hand, reports suggested that the microevolution, speciation and macroevolution in rhizobia itself was driven by host selection pressure [62]. Similar to AMF, rhizobial growth, and association are kindled by host-secreted flavonoids. In response, rhizobia releases Nod factors and LCOs that activate the CSSP pathway in host plants. As a result, structural reorientation of roots takes place followed by the entry of rhizobia into the root interior, which leads to the establishment of the bacteria within a highly specialized structure, the ‘symbiosome’. The symbiosome is referred to as the hub of nutrient exchange between both the associated partners [61]. Apart from leguminous and one leguminous plant, the nodule is also found in actinorrhizal plants of almost 260 species belonging to the Fabales, Rosales, and Curcurbitales order [63]. Research works highlight the plant-nodule signaling in Frankia to be similar to that of plant-rhizobia interaction. However, cluster I and III Frankia that lack the core nod ABC nodulation genes produce hydrophilic chitin-resistant molecules, which are known to trigger calcium oscillations leading to the upregulation of the CSSP pathway [64] (Fig. 1). The cognate effector protein receptors of Frankia are not yet reported from host plants. Besides, symbiosomes of plant-rhizobia interaction have replaced plant-infection thread interaction in plant-Frankia interaction. Although, experimental reports have provided authentications on the changes that occur during different types of symbiosis discussed briefly above, why and how these alterations in symbiotic behavior occurred in later time spans conserving the ancient one in place is still an enigma. Moreover, the emerging concept of latent defense response (LDR), which is conditionally stimulated by non-pathogenic factors (NPFs) secreted by some microbes to impose a checkpoint on mutualists and commensals in entering into any condition-specific incompatible interaction with the host also needs to be categorically explored prior to utilizing symbiotic microbe mediated soil supplements for agricultural improvement [65].
Fig. (1)) Schematic diagram showing an overview of the major events during the evolution of plant terrestrialization and its interaction with diverse groups of microorganisms. Figure 1 shows the following features 1. The origin of microbes on Earth was about 3.4 billion years ago. 2. The origin of aquatic plants. 3 and 4. Origin of land plants from Charophytes. 5. Colonization of land plants with microbes of different behavioral patterns like 6. mycorrhizae 7. commensals 8. Nodulating rhizobacterias and 9. pathogens. The figure also shows the diagrammatic representation of the common symbiotic signaling pathway (CSSP) and plant-pathogenic interaction pathway.Molecular Evolution of the Arms Race of Plant Versus Pathogen
Very interestingly and intriguingly, the transition of plant-microbe interaction to plant-pathogen encounter dates back to approximately 100 million years ago, when plants were deeply engaged with symbiotic organisms for their growth and development. The origin of land plants documents the association of plants with bacteria and fungi. Moreover, the molecular dissection of CSSP shows that symbiosis occurs while the immune signaling pathway remains in suppression. Thus, it can be quite wisely deciphered that symbiosis and plant antagonism were simultaneous events to have occurred in the evolutionary pathway of plant-microbe interaction. Analytical reports based on ancient molecular clocks strongly support that the plant-pathogen encounter made significant changes in both the interacting partners that led to unending cycles of co-evolution in both the host and its pathogen. This phenomenon is termed ‘Red Queen’ dynamics in the field of plant interaction biology [66]. Red Queen dynamics is broadly classified into three types: 1) Fluctuating Red Queen, which occurs when a rare genotype of the host within a given population shows enhanced resistant features as compared to normal members exhibiting a phenomenon referred to as the negative-frequency dependent selection. Such negative-frequency-dependent selection brings about allelic fluctuations in both interacting partners and maintains genetic diversity. Usually, such type of negative-frequency dependent selection is imposed upon on host and pathogen due to several ecological and epidemiological factors [67]. 2) Escalatory Red Queen, where both host and pathogen are engaged in a continuous tug of war to overpower each other, while the last one 3) Chase Red Queen, where the host puts constant tough efforts to tone down the intensity of infection while pathogens make steady manipulations to strengthen their establishment within the host interior. Reports suggest that all the above frequency-based selection and/or arms race selection bring about dynamic changes and coerce co-evolutionary shifts, which often culminate in a sweep of a particular population of either the host and/or the pathogen [68].
Understanding of molecular dynamics of plant pathogen interaction has substantially grown over the years where logical interpretation based on experimental data was obtained. Dyakov et al. offered a wealth of information regarding the molecular dialogue between plant and pathogen interaction that involved host and non-host versus pathogen interaction, elicitors versus suppressors, all of which expanded the understanding of the logic of plant-parasite interaction [69]. Accordingly what is well established in present times is that the diversity in plant-pathogen interaction was the effect of terrestrialization and its subsequent exposure to dynamic climatic conditions [70]. The stationary condition of land plants compelled them to get exposed to diverse microorganisms, out of which many did not aid in providing ecosystem services and transformed into pathogens at later periods. Some acted as commensals in lending neither support nor antagonism to the host but benefitted from the host, a relationship termed as ‘no effect commensalism’. Besides, another more specialized relationship is also known to occur where balanced costs and benefit are provided by the host to the commensals. However, commensalism is believed to be not a single type of interaction but rather a collection of interactions that are ecologically and co-evolutionarily governed [21]. However, the criterion, and dynamics of deciding the balance versus cost in the commensal relationship are still open-ended questions. The theories of plant-pathogen interaction have universally stated that plants lack adaptive immunity; instead have two-tier innate immunity. Such immune mechanisms not only take part in vigorous surveillance but also restrict a major fraction of harmful intruders at the entry point [71]. The surveillance system is maintained and activated when microbe-associated molecular patterns (MAMPs) and/or microbial infection-induced damage-associated molecular patterns (DAMPs) of the host are identified by pattern recognition receptors (PRRs) of the host [72]. The MAMP/DAMP recognition by PRR triggers the activation of Pattern Triggered Immunity (PTI), which is reported to adequately tackle the invasion of a large number of pathogens [73]. Receptor-like kinases (RLKs) and Receptor-like proteins (RLPs) work as PRRs [70]. Structurally RLKs have an extracellular domain, a single-span transmembrane domain, and an intracellular kinase domain, while RLPs having similar features lack kinase domain. The extracellular domain of PRRs, which governs ligand binding is highly variable and is known to possess leucine-rich repeats (LRR), lysine motif (LysM), lectin, epidermal growth factor (EGF) like domain, etc [74]. PRRs are capable of binding with diverse extracellular ligands, which co-activate and associate with several receptor-like cytoplasmic kinases (RLCKs) and stimulate downstream calcium-dependent protein kinases (CDPKs) and mitogen-activated protein kinase (MAPK) signaling cascades leading to the establishment of PTI [75].
However, a limited number of pathogens dodge the host’s first line of defense (PTI) and make attempts to gain over the host's immunity by secreting effector molecules and causing effector-triggered susceptibility (ETS) [71]. As a counter-defense mechanism, the hosts recruit several resistant proteins (R proteins), which are known to be the translational products of R genes. R genes are known to have characteristic structural resemblance in coding for nucleotide binding sites and leucine-rich repeats (NBS-LRR). In most cases, the effector directly binds to the R protein of the host. However, in rare cases, the effector proteins indirectly interact with some R protein guardees or decoy molecules which are monitored by the cognate R protein, and indirectly activate downstream effector-triggered immunity (ETI) [76]. Such an indirect interaction model is referred to as the ‘Decoy/Guardee’ Model of Immune signaling. Both direct and indirect interaction of pathogen effectors and host R protein culminates in stimulating ETI. ETI regulates hypersensitive responses (HR) and programmed cell death (PCD) at the host interior which restricts further pathogenic ingress [71]. Apart from imparting localized resistance response, ETI is also known to induce systemic signals by producing mobile signaling molecules such as methyl salicylic acid (MeSA), azelaic acid, and glycerol 3 phosphate (G3P) which are transferred to distant places to provide systemic acquired resistance (SAR) [77]. These SARs help in the production of pathogenesis-related proteins (PR proteins) having antimicrobial activity that endows the host in acquiring immune memory and protecting itself from future pathogenic attack [77]. RNA interference (RNAi) controls defense against viral infection. Doubled-stranded RNA (dsRNA), which are found as the replicative intermediates of viruses are targeted by Dicer-like proteins (DCLs), which produce viral small interfering RNAs (siRNAs). These siRNA are loaded with Argonaute proteins (AGO), which are targeted for viral mRNA cleavage and thus triggering anti-viral immunity [78] (Fig. 1).
Plant RLKs and RLCKs, closely related to Drosophila Pelle proteins and animal cytoplasmic kinases are grouped under RLK/Pelle family. The RLKs and RLCKs are clustered within a single group although RLCKs lack the extracellular transmembrane domain. This suggests that the RLCKs have either originated from RLKs (by deleting the extracellular domain) or might be the ancestors of RLKs that acquired an extracellular transmembrane domain as per the demand of the situation [79]. Both RLKs and RLCKs are known to have originated in Charophyta. Although homologues of these receptors were found in primitive members of Glaucophyta, Rhodophyta, and Chlorophyta, their structural similarity fails to identify them as appropriate ancestors of RLS/RLCKs of later-day land plants. NLR protein is also reported to have originated from Charopytes suggesting that the plant pathogen interaction components meant for PTI and ETI coevolved under aquatic conditions, especially in members that were possibly destined to undergo reprogramming to adapt to land habitats. However, the origin of plant immune response against viral pathogens probably occurred much earlier in aquatic habitats in members of Glaucophyta, Rhodophyta, and Chlorophyta [80].
ECOLOGICAL-DRIVEN EVOLUTION OF PLANT-MICROBE INTERACTION
Evolution makes changes in ecology or ecology controls the course of evolution is still a long-standing question. Previous research emphasized the fact that evolution occurred in long time scales with changes in genetic makeup that brought about changes in its ecological system. However, present-day understandings emphasize the temporal and spatial changes and their ecological contexts to be the crucial drivers of any and every change in an organism’s structure and behavior that ultimately accounts for the evolution of the organism. Modern theories of Price Equation partition ecological and evolutionary effects based on the ecological variables. Such equations are known to decide the rules of Eco-Evo interaction [81]. For example, the evolution of inducible defenses such as the production of secondary metabolites during the ecological context of herbivory is known to alter the litter composition, which is grossly different during the absence of herbivory. Hence, the ecological situation caused by herbivory on one hand alters evolutionary trends (evolves the production of secondary metabolites), while on the other hand, it modifies ecological parameters by changing soil litter composition [82]. In recent times, the Eco-Evo relationship has received strong support in understanding the belowground and above-ground interactions beyond the one-to-one concept. Thus the fundamental role of microbiome in governing the Eco-Evo interaction of plant-microbe association has also been realized in recent times [81]. The microbiome is known to affect the evolution of a plant even at the micro level. Microbiome directly helps in the increment of plant performance with respect to its growth, development, and resilience against stress factors both abiotic and biotic. In response, plants regulate mutualism by manipulating the association with beneficial microbial partners by making appropriate partner choices and controlling partner fidelity [83]. Although the degree of relatedness of interaction between plants and their symbionts over longer time scale and seasons is poorly understood, nevertheless, the association if and when exists for longer periods for several cycles supports the evolution of the host accordingly so that the association also remains conserved over generations [84]. Both vertical transmission and horizontal transmission of the microbiome are known to support plant fidelity [85]. How plants choose their beneficial partners from a mixture of diverse microbial communities offering the same resources and lying in close proximity to the plants is still not well understood. Reports suggest that partner choice probably occurs at two levels. At level, 1) plants preferentially allocate their resources to those plant organs that harbor more microbial communities of a cooperative nature, and at level 2), plants allocate resources specifically to those microbial taxa that offer more cooperation within a single plant organ [86]. The understanding of the gradually growing symbiogenesis is believed to provide a concrete understanding of the genetic control over different symbiotic and biocenotic interactions in the future [87].
Similar to mutualistic interaction, the microbiome is known to control antagonistic interactions as well. Microbiome, and much categorically the plant holobiont is known to act as a supplementary barrier that maintains a strong vigil on the microbes that attempt to sneak into the plant interior [88]. Thus any addition or alteration in the microbiome is likely to bring changes in the plant-pathogen relation. The holobiont that helps the plant in providing resistance and resilience to abiotic and biotic stress is preferably retained over the generations and is thought to be evolved. On the other hand, the plant that reprograms itself to maintain the growth and fecundity of its holobiont is also considered to be coevolved [13]. However, the co-evolution of both the plant holobiont is linked to its ecological parameters, which are known to be largely altered due to changes in climatic conditions [89]. Change in climatic situations causes changes in the allogenic parameters of soil and autogenic properties of species-species interaction thus altering the entire microbiome, which may attain stability if the climatic conditions prevail [90]. On the contrary, plant genotypes and their signature genetic and biochemical components also shape the structure and function of the microbiome [91]. Besides, ecological processes such as dispersal, selection, ecological drift, diversification, and domestication are also reported to alter microbiome structure and function and directly impact plant-pathogen interaction [13]. However, how these alterations caused by ecological drivers can be tackled and judicially exploited to enhance plant productivity in the era of unpredictable climate change is still an unexplored area.
CONCLUSION
Over the last several decades, enormous additions have been made to the understanding of plant-microbe interactional studies. Even then, large knowledge gaps still exist, specifically in areas regarding 1) why and how a potential host plant selects out the most beneficial microbial partner from a pool of functionally similar microbes with the same affinities for a particular host? 2) How and why does a symbiont make behavioral transformation and convert it into a commensal or a pathogen? 3) How does a host and its associated holobiont sense climatic disturbances? Supporting the notion that ecology governs evolution, 4) how long is an exposure to a particular ecological condition such as drought, temperature stress, salinity, metal toxicity, biotic attack, etc, necessary to bring about sustainable evolutionary changes in the host and its surrounding microbiome, 5) Is the ecology driven epigenetic change heritable for several forthcoming generations of both the host and its interacting partner/s? 6) What happens to the already acquired genetic change and how do the individuals react if the ecological conditions are reverted back?
According to previous research, evolution was believed to be a random process that occurred by random genetic drift and mutations that were naturally selected over time. However, in recent times, researchers of evolutionary biology claim it to be a bias and argue that evolution is not a random process and is governed by either intragenomic combinations or ecological drivers [92]. Thus, the above sections summarize the importance and influence of ecological dynamics in the evolution of plants and their interacting partners of the holobiont as well as the microbiome. However, predicting the unexpected alterations of abiotic ecological factors that bring gross changes in biotic factors and their interrelationships is still a steep challenge for scientists. Experimental evolution (EE) has, however, emerged as a promising tool for studying the life and behavior of small organisms mainly microbes, with controlled generation times under specified laboratory conditions [93]. EE models have thus made substantial advancements in analyzing the role of plant-microbe interaction and decoding its probable evolutionary trends [93]. However, more EE models based on variable ecological parameters could serve as a reliable alternative method to make prior predictions on the impact of climatic shifts on ecology and evolution. Hence designing and critically analyzing the EE models is expected to open up a new dimension in the area of understanding the evolution of plant microbe interaction.
