New Phytologist - 2018 - Han - Origin and evolution of the plant immune system

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<p>Tansley review</p><p>Origin and evolution of the plant immune</p><p>system</p><p>Author for correspondence:</p><p>Guan-Zhu Han</p><p>Tel: +86 25 85891836</p><p>Email: guanzhu@njnu.edu.cn</p><p>Received: 27 August 2018</p><p>Accepted: 2 November 2018</p><p>Guan-Zhu Han1,2</p><p>1Jiangsu Key Laboratory for Microbes and Functional Genomics, College of Life Sciences, Nanjing Normal University, Nanjing,</p><p>Jiangsu 210023, China; 2College of Life Sciences, Shandong Normal University, Jinan, Shandong 250014, China</p><p>Contents</p><p>Summary 70</p><p>I. Introduction 70</p><p>II. Ancient associations between plants and microbes 72</p><p>III. Evolutionary dynamics of plant–pathogen interactions 74</p><p>IV. Evolutionary signature of plant–pathogen interactions 74</p><p>V. Origin and evolution of RLK proteins 75</p><p>VI. Origin and evolution of NLR proteins 77</p><p>VII. Origin and evolution of SA signaling 78</p><p>VIII. Origin and evolution of RNA-based defense 79</p><p>IX. Perspectives 79</p><p>Acknowledgements 80</p><p>References 80</p><p>New Phytologist (2019) 222: 70–83</p><p>doi: 10.1111/nph.15596</p><p>Keywords: comparative genomics,molecular</p><p>arms race, NBS-LRR protein, phylogenetic</p><p>analysis, plant immune system, receptor-like</p><p>kinase, Red Queen dynamics.</p><p>Summary</p><p>Microbes have engaged in antagonistic associationswith plants for hundreds ofmillions of years.</p><p>Plants, in turn, have evolved diverse immune strategies to combat microbial pathogens. The</p><p>conflicts between plants and pathogens result in everchanging coevolutionary cycles known as</p><p>‘Red Queen’ dynamics. These ancient and ongoing plant–pathogen interactions have shaped</p><p>the evolution of both plant and pathogen genomes.With the recent explosion of plant genome-</p><p>scale data, comparative analyses provide novel insights into the coevolutionary dynamics of</p><p>plants and pathogens. Here,we discuss the ancient associations between plants andmicrobes as</p><p>well as the evolutionary principles underlying plant–pathogen interactions. We synthesize and</p><p>review the current knowledge on the origin and evolution of key components of the plant</p><p>immune system. We also highlight the importance of studying algae and nonflowering land</p><p>plants in understanding the evolution of the plant immune system.</p><p>I. Introduction</p><p>Plant pathogens employ diverse strategies to attack plants and</p><p>impair plant growth and reproduction. Unlike vertebrates, plants</p><p>lack mobile immune cells and an adaptive immune system. Plants</p><p>mainly rely on two interconnected tiers of the innate immune</p><p>system to perceive and respond to pathogen infections (Fig. 1;</p><p>Jones &Dangl, 2006; Boller & Felix, 2009; Thomma et al., 2011;</p><p>Spoel & Dong, 2012). One uses cell surface pattern-recognition</p><p>receptors (PRRs) to recognize microbe-associated molecular</p><p>patterns (MAMPs) present in a large group of microbes and</p><p>host-derived damage-associated molecular patterns (DAMPs)</p><p>(Boller & Felix, 2009). The other uses disease resistance (R)</p><p>proteins to respond to effector molecules that are secreted by</p><p>pathogens to help establish successful infections and suppress plant</p><p>immunity (Upson et al., 2018).</p><p>The perception of MAMPs or DAMPs by PRRs activates</p><p>defense against invading pathogens, termed as pattern-triggered</p><p>immunity (PTI) (Jones & Dangl, 2006; Zipfel, 2014). Receptor-</p><p>like kinases (RLKs, also known as receptor kinases) and receptor-</p><p>70 New Phytologist (2019) 222: 70–83 � 2018 The Author</p><p>New Phytologist� 2018 New Phytologist Trustwww.newphytologist.com</p><p>Review</p><p>https://orcid.org/0000-0002-8352-7726</p><p>https://orcid.org/0000-0002-8352-7726</p><p>http://crossmark.crossref.org/dialog/?doi=10.1111%2Fnph.15596&domain=pdf&date_stamp=2019-01-07</p><p>like proteins (RLPs) have been identified to function as PRRs</p><p>(Boller & Felix, 2009). Some RLKs and RLPs might play essential</p><p>roles in plant development, resistance to abiotic stresses and</p><p>symbiosis (Tang et al., 2017). A canonical RLK is characterized by</p><p>an extracellular domain involved in ligand perception, a single-pass</p><p>transmembrane domain and an intracellular kinase domain (Couto</p><p>& Zipfel, 2016; Zipfel & Oldroyd, 2017). RLPs are essentially</p><p>RLKs that lack the kinase domain (Zipfel, 2014; Couto & Zipfel,</p><p>2016; Zipfel & Oldroyd, 2017). PRRs possess highly variable</p><p>extracellular domains, such as leucine-rich repeat (LRR), lysine</p><p>motif (LysM), lectin and epidermal growth factor (EGF)-like</p><p>domains, and thus can recognize a wide range of ligands (Fig. 2; Yu</p><p>et al., 2017). On ligand binding, PRRs form complexes with co-</p><p>receptors that share similar extracellular domains (Ranf, 2017;</p><p>Zipfel & Oldroyd, 2017). Association and activation of receptor-</p><p>like cytoplasmic kinases (RLCKs) with PRR complexes is involved</p><p>in relayingPTI signaling (Yu et al., 2017;Zipfel&Oldroyd, 2017).</p><p>PRR complexes trigger the activation of calcium-dependent</p><p>protein kinases (CDPKs) and mitogen-activated protein kinase</p><p>(MAPK) cascades, which results in transcriptional reprograming to</p><p>establish PTI (Couto & Zipfel, 2016; Yu et al., 2017).</p><p>To establish successful infections, pathogens have evolved a</p><p>diverse repertoire of effectors that are delivered into plant cells to</p><p>interfere with PTI (Jones & Dangl, 2006; Boller & Felix, 2009).</p><p>The pathogen effectors are usually specific to individual pathogens</p><p>and are not generally conserved in microbial groups above the</p><p>family level (Boller & Felix, 2009). To counter this infection</p><p>strategy, plants use R proteins to respond to effectors either through</p><p>direct binding or sensing perturbations of host molecules (also</p><p>known as guardees and decoys) by pathogen effectors (see Kourelis</p><p>& van der Hoorn, 2018 for a detailed review on the recognition</p><p>mechanisms). Recognition of pathogen effectors results in effector-</p><p>triggered immunity (ETI) (Jones & Dangl, 2006; Spoel & Dong,</p><p>2012). Most plant R genes encode intracellular nucleotide</p><p>binding-site leucine-rich repeat (NLR, also known as NBS-LRR)</p><p>proteins (Fig. 2). ETI usually induces programmed cell death at the</p><p>infection site, known as the hypersensitive response (HR), and thus</p><p>locally limits pathogen spread (Jones & Dangl, 2006).</p><p>ETI can induce the production of mobile immune signals in</p><p>plants, such as methyl salicylic acid (MeSA), azelaic acid and</p><p>glycerol-3-phosphate (G3P), which are transported from the</p><p>infection site to systemic uninfected tissues (Fig. 1; Spoel &Dong,</p><p>2012; Fu & Dong, 2013). The perception of these signals in</p><p>uninfected tissues induces the accumulation of SA and mediates</p><p>massive transcriptional programming (Spoel &Dong, 2012; Fu&</p><p>Dong, 2013). This induced immune mechanism is termed</p><p>systemic acquired resistance (SAR). Ultimately, it leads to the</p><p>production of pathogenesis-related (PR) proteins with antimicro-</p><p>bial activity, which protects plants from subsequent pathogen</p><p>attacks (Spoel & Dong, 2012; Fu & Dong, 2013). In Arabidopsis</p><p>O</p><p>OH</p><p>OH</p><p>MAMP</p><p>RLK</p><p>PTI response</p><p>Effectors</p><p>NLR ETI</p><p>response</p><p>MeSA</p><p>G3P</p><p>Azelaic acid</p><p>Salicylic acid</p><p>SA signaling</p><p>NPRmiR482/2118</p><p>dsRNA</p><p>Viruses</p><p>Virus replication</p><p>DCL</p><p>AGO</p><p>Suppressors</p><p>RNA silencing</p><p>Fig. 1 A brief overview of the plant immune system. Green boxes represent plant cells. Pathogen-derived components are labeled in orange. Plant immunity-</p><p>related proteins and miRNAs are labeled in blue (the deeper the color, the older the component). The perception of microbe-associated molecular patterns</p><p>(MAMPs) by receptor-like kinases (RLKs) activates the pattern-triggered immunity (PTI) response. Pathogens deliver awide variety of effectors into plant cells</p><p>to interfere with plant PTI. 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Nature</p><p>543: 328–336.</p><p>� 2018 The Author</p><p>New Phytologist� 2018 New Phytologist Trust</p><p>New Phytologist (2019) 222: 70–83</p><p>www.newphytologist.com</p><p>New</p><p>Phytologist Tansley review Review 83</p><p>14698137, 2019, 1, D</p><p>ow</p><p>nloaded from</p><p>https://nph.onlinelibrary.w</p><p>iley.com</p><p>/doi/10.1111/nph.15596 by M</p><p>ozam</p><p>bique H</p><p>inari N</p><p>PL</p><p>, W</p><p>iley O</p><p>nline L</p><p>ibrary on [31/08/2024]. See the T</p><p>erm</p><p>s and C</p><p>onditions (https://onlinelibrary.w</p><p>iley.com</p><p>/term</p><p>s-and-conditions) on W</p><p>iley O</p><p>nline L</p><p>ibrary for rules of use; O</p><p>A</p><p>articles are governed by the applicable C</p><p>reative C</p><p>om</p><p>m</p><p>ons L</p><p>icense</p><p>producing viral siRNAs. Viral siRNAs are loaded in Argonaute (AGO) proteins to guide viral RNA cleavages and thus</p><p>restrict viral replication. Viruses evolve viral suppressors to avoid RNA silencing.</p><p>� 2018 The Author</p><p>New Phytologist� 2018 New Phytologist Trust</p><p>New Phytologist (2019) 222: 70–83</p><p>www.newphytologist.com</p><p>New</p><p>Phytologist Tansley review Review 71</p><p>14698137, 2019, 1, D</p><p>ow</p><p>nloaded from</p><p>https://nph.onlinelibrary.w</p><p>iley.com</p><p>/doi/10.1111/nph.15596 by M</p><p>ozam</p><p>bique H</p><p>inari N</p><p>PL</p><p>, W</p><p>iley O</p><p>nline L</p><p>ibrary on [31/08/2024]. See the T</p><p>erm</p><p>s and C</p><p>onditions (https://onlinelibrary.w</p><p>iley.com</p><p>/term</p><p>s-and-conditions) on W</p><p>iley O</p><p>nline L</p><p>ibrary for rules of use; O</p><p>A</p><p>articles are governed by the applicable C</p><p>reative C</p><p>om</p><p>m</p><p>ons L</p><p>icense</p><p>thaliana, both the nonexpresser of PR genes 1 (NPR1) protein and</p><p>NPR3/4 proteins bind SA and serve as SA receptors (Ding et al.,</p><p>2018). NPR1 protein andNRP3/4 proteins act as a transcriptional</p><p>co-activator and transcriptional co-repressors, respectively, and</p><p>play opposite roles in transcriptional regulation of defense gene</p><p>expression (Ding et al., 2018).</p><p>RNA interference (RNAi; or RNA silencing) functions as a</p><p>defense mechanism against viral infections in plants (Fig. 1; Ding,</p><p>2010; Couto & Zipfel, 2016). Double-stranded RNA (dsRNA)</p><p>replicative intermediates of RNA viruses are processed by Dicer-</p><p>like (DCL) proteins, producing viral small interfering RNAs</p><p>(siRNAs). Viral siRNAs are loaded in Argonaute (AGO) proteins</p><p>to guide viral mRNA cleavage and induce RNA-based antiviral</p><p>immunity (Ding, 2010; Couto & Zipfel, 2016). Moreover, small</p><p>RNAs have recently been suggested to play important roles in</p><p>regulating the expression of R genes as well as PTI and ETI</p><p>signaling pathways in plants (Pumplin & Voinnet, 2013).</p><p>In this review,we focus on the origin and evolution of these plant</p><p>immune strategies. We first discuss the ancient associations</p><p>between plants andmicrobes. Second, we consider the evolutionary</p><p>principles underlying plant–pathogen interactions and how to</p><p>examine the evolution of plant–pathogen interactions at the</p><p>molecular level. Lastly, we analyze and discuss the origin and</p><p>evolutionary dynamics of key components of the plant immune</p><p>system.</p><p>II. Ancient associations between plants and microbes</p><p>When did plants establish symbiotic associations withmicrobes? In</p><p>this review, we use the collective meaning of symbiotic association:</p><p>it represents a long-term ecological interaction that could range</p><p>from mutualism to parasitism. The appearance of visible disease</p><p>symptoms in plants is merely an extreme outcome of the</p><p>continuum of plant–microbe associations (Bulgarelli et al.,</p><p>2013). The nature of symbiotic associations, antagonistic or</p><p>synergetic, between plants and microbes might not be easily</p><p>demonstrated, especially in fossils.</p><p>Bacteria were around for c. 2 billion years before the</p><p>emergence of plants (Archaeplastida; Box 1) c. 1.6 billion years</p><p>ago (Parfrey et al., 2011; Kumar et al., 2017; Betts et al., 2018).</p><p>While the precision of the dates estimated from molecular</p><p>clocks should be taken with caution (Graur & Martin, 2004;</p><p>Hedges & Kumar, 2004), they nevertheless provide important</p><p>information for comparing the time scales of the evolution of</p><p>different lineages. Land plants host a remarkable diversity of</p><p>bacteria, and many bacteria can cause various diseases in land</p><p>plants (Bulgarelli et al., 2013; Bragina et al., 2014). Similarly,</p><p>there are diverse bacterial communities in algae. For example,</p><p>the green algae Ulva australis and Caulerpa taxifolia host</p><p>hundreds of bacterial species (Burke et al., 2011; Arnaud-</p><p>Haond et al., 2017). Bacteria might also become pathogenic in</p><p>algae. Infection by the bacterium Pseudomonas protegens inhibits</p><p>the growth of the green alga Chlamydomonas reinhardtii (Aiyar</p><p>et al., 2017). It seems reasonable to hypothesize that plants have</p><p>encountered and established symbiotic (including antagonistic)</p><p>associations with bacteria since the emergence of plants. Indeed,</p><p>the origin of plants is a result of engulfing and integrating a</p><p>cyanobacterium-like prokaryote by the common ancestor of</p><p>plants (Box 1; Gould et al., 2008; de Vries & Gould, 2018).</p><p>The kingdom Fungi was estimated to have arisen c. 1 billion</p><p>years ago (Parfrey et al., 2011; Chang et al., 2015; Tedersoo et al.,</p><p>2018). The earliest fungi were primarily aquatic, and fungi</p><p>colonized terrestrial environments long before plants (Heckman</p><p>et al., 2001; James et al., 2006). Land plants can establish ecological</p><p>associations with diverse fungal lineages (James et al., 2006; Feijen</p><p>et al., 2018). The appearance of the arbuscular mycorrhizal</p><p>symbiosis with fungi has been proposed to be crucial in facilitating</p><p>colonization of terrestrial environments by plants (Humphreys</p><p>et al., 2010; Delaux et al., 2015). The fossil records for plant–</p><p>fungus associations can be dated back to 407Ma (Strullu-Derrien</p><p>et al., 2018). Fungi have long been known to cause diseases in land</p><p>plants, including liverworts and mosses (Carella & Schornack,</p><p>2018). Many so-called ‘early-branching lineages’ of Fungi (note</p><p>that the terms ‘basal’ or ‘early-branching’ might cause some</p><p>misinterpretations (Crisp & Cook, 2005); see also Box 1), such as</p><p>Chytridiomyceta and Aphelidiomycota, contain species that</p><p>establish either parasitic or mutualistic associations with green</p><p>algae (Letcher et al., 2013; Picard et al., 2013; Tedersoo et al.,</p><p>2018). Interestingly, most known Aphelidiomycota species, whose</p><p>diversity was estimated to have arisen c. 500Ma (Tedersoo et al.,</p><p>2018), are intracellular parasites of green algae.Moreover, enzymes</p><p>for digesting plant cell-wall components were shared between</p><p>Dikarya and Chytridiomycota species, indicating ancient aquatic</p><p>fungi evolved to extract nutrients from plants (Chang et al., 2015;</p><p>Berbee et al., 2017). Therefore, fungi might have been associated</p><p>with plants for hundreds of millions of years, probably since the</p><p>origin of fungi (Letcher et al., 2017; Tedersoo et al., 2018).</p><p>Oomycetes belong to the lineage of Heterokonts (commonly</p><p>referred to as Stamenopiles) within the kingdom Chromista</p><p>(Beakes et al., 2012). Oomycetes are symbionts and pathogens of a</p><p>wide range of eukaryotes, including plants. Fossil records provide</p><p>clear evidence for the association between oomycetes and plants in</p><p>the Carboniferous (c. 315Ma) (Strullu-Derrien et al., 2011). The</p><p>oomycete pathogens could have infected many land plants,</p><p>including mosses and liverworts (Carella & Schornack, 2018).</p><p>Extracellular domain TM Kinase</p><p>RLP RLCK</p><p>RLK</p><p>NLR NB-ARC LRR</p><p>Fig. 2 Domain architecture of RLKs and NLRs. A canonical RLK is</p><p>characterizedby anextracellular domain, a single-pass transmembrane (TM)</p><p>domain and an intracellular kinase domain. Receptor-like proteins (RLPs,</p><p>gray box) are essentially RLKs that lack the kinase domain. Receptor-like</p><p>cytoplasmic kinases (RLCKs, blue box) only have a cytoplasmic kinase</p><p>domain that belongs to the RLK/Pelle family as RLKs. RLKs have variable</p><p>extracellular domains, such as LRR, LysM, lectin and EGF-like domains. A</p><p>canonical NLR is characterized by an NB-ARC domain and a series of LRRs.</p><p>There might be an additional domain (dashed box), such as TIR, RPW8,</p><p>Pkinase or DUF676, at the N-terminus.</p><p>New Phytologist (2019) 222: 70–83 � 2018 The Author</p><p>New Phytologist� 2018 New Phytologist Trustwww.newphytologist.com</p><p>Review Tansley review</p><p>New</p><p>Phytologist72</p><p>14698137, 2019, 1, D</p><p>ow</p><p>nloaded from</p><p>https://nph.onlinelibrary.w</p><p>iley.com</p><p>/doi/10.1111/nph.15596 by M</p><p>ozam</p><p>bique H</p><p>inari N</p><p>PL</p><p>, W</p><p>iley O</p><p>nline L</p><p>ibrary on [31/08/2024]. See the T</p><p>erm</p><p>s and C</p><p>onditions (https://onlinelibrary.w</p><p>iley.com</p><p>/term</p><p>s-and-conditions) on W</p><p>iley O</p><p>nline L</p><p>ibrary for rules of use; O</p><p>A</p><p>articles are governed by the applicable C</p><p>reative C</p><p>om</p><p>m</p><p>ons L</p><p>icense</p><p>However, it remains unclear how oomycetes that infect land plants</p><p>originated (Selosse et al., 2015). Parasitism might evolve from</p><p>either algal parasites or from land saprotrophic oomycetes (Selosse</p><p>et al., 2015). Besides land plants, oomycetes</p><p>can infect both green</p><p>and red algae (Li et al., 2010). However, the genera (such as</p><p>Olpidiopsis) that infect red algae and the genera (such as</p><p>Phytophthora) that infect land plants do not form a monophyletic</p><p>group (Beakes et al., 2012), suggesting possibly independent</p><p>origins of plant parasitism by oomycetes. Nevertheless, current</p><p>evidence clearly suggests ancient associations between oomycetes</p><p>and plants.</p><p>Most known viruses have been found in angiosperms, and very</p><p>few viruses have been characterized in plants outside angiosperms.</p><p>Most of these known angiosperm viruses have RNA or single-</p><p>stranded DNA (ssDNA) genomes. Meta-transcriptomic analysis</p><p>suggests the presence of RNA viruses in plants other than</p><p>angiosperms (Mushegian et al., 2016). Moreover, green algae can</p><p>be infected by giant viruses with large double stranded DNA</p><p>(dsDNA) genomes (Van Etten, 2003). Viruses occasionally</p><p>integrate into host genomes, forming endogenous viral elements</p><p>(EVEs). EVEs provide ‘molecular fossils’ for studying the deep</p><p>history of viruses. Endogenous ssDNA, RNA, dsDNA and reverse-</p><p>transcribing dsDNA (dsDNA-RT) viruses have been identified</p><p>within the genomes of a wide range of plants (Aiewsakun &</p><p>Katzourakis, 2015). Genes of giant viruses were identified within</p><p>the genomes of several land plants, suggesting dsDNA viruses</p><p>infected land plants (Filee, 2014; Maumus et al., 2014). Endoge-</p><p>nous Caulimoviridae (also known as plant pararetroviruses), a</p><p>group of dsDNA-RT viruses, were identified in a wide range of</p><p>euphyllophytes, including angiosperms, gymnosperms and ferns</p><p>(Gong & Han, 2018). Evolutionary analyses suggest that plant</p><p>pararetroviruses invaded host genomes c. 100–200Ma. All these</p><p>data indicate diverse viruses have been infecting plants for millions</p><p>of years.</p><p>Box 1 Evolution of plants</p><p>Embryophyta</p><p>(land plants)</p><p>Tracheophyta</p><p>Hornworts</p><p>Mosses</p><p>Liverworts</p><p>Bryophyta</p><p>Streptophyta</p><p>Viridiplantae</p><p>(green plants)</p><p>Archaeplastida</p><p>CharophytaZygnematophyceae</p><p>Coleochaetophyceae</p><p>Charophyceae</p><p>Klebsormidiophyceae</p><p>Chlorokybophyceae</p><p>Mesostigmatophyceae</p><p>Chlorophyta</p><p>Rhodophyta</p><p>Glaucophyta</p><p>The Archaeplastida is a monophyletic group of plastid-bearing eukaryotes. The plastids of Archaeplastida originated through a single, ancient primary</p><p>endosymbiosiswhereby a free-living cyanobacteriumwas takenupby aheterotrophic eukaryote (Archibald, 2015;Nowack&Weber, 2018; deVries&</p><p>Gould, 2018). Over time, hundreds of genes were transferred from the endosymbiont to the host nucleus through endosymbiotic gene transfer</p><p>(Archibald, 2015; Nowack & Weber, 2018). The Archaeplastida comprises three major clades: Glaucophyta (glaucophyte algae), Rhodophyta (red</p><p>algae) and Viridiplantae (green plants). Viridiplantae diverged into two lineages, Chlorophyta and Streptophyta (Leliaert et al., 2012). Chlorophyta</p><p>comprisesmostdescribedgreenalgae, andStreptophyta includesCharophyta,aparaphyletic groupof freshwateralgae, andEmbryophyta (landplants)</p><p>(Leliaert et al., 2012). Although multiple lineages of Viridiplantae and Rhodophyta colonized terrestrial environments independently, land plants</p><p>originated through a single lineage of charophytes (Delwiche & Cooper, 2015; de Vries & Archibald, 2018). Recent phylogenomic analyses provide</p><p>strong evidence for a sister group relationship between the charophyte class Zygnematophyceae and land plants (Wickett et al., 2014). Regarding the</p><p>relationship within land plants, liverworts, mosses and hornworts (known as Bryophyta) were widely thought to be successive sister groups to</p><p>Tracheophyta (vascular plants). However, recent phylogenomic analyses unite liverworts and mosses, but the relationship between hornworts and</p><p>other land plants remains uncertain (Wickett et al., 2014; Puttick et al., 2018). Some relationships within land plants remain enigmatic (Wickett et al.,</p><p>2014). Bryophytes are often referred to as ‘basal’, ‘early-diverging’ or ‘early-branching’ land plants. These terms are misleading and might cause</p><p>misinterpretation of phylogenetic trees, because the so-called ‘early-branching’ lineages and their sister groups originated simultaneously from their</p><p>most recent common ancestor and the ‘early branching’ lineages do not signify ancestral traits (Crisp & Cook, 2005).</p><p>� 2018 The Author</p><p>New Phytologist� 2018 New Phytologist Trust</p><p>New Phytologist (2019) 222: 70–83</p><p>www.newphytologist.com</p><p>New</p><p>Phytologist Tansley review Review 73</p><p>14698137, 2019, 1, D</p><p>ow</p><p>nloaded from</p><p>https://nph.onlinelibrary.w</p><p>iley.com</p><p>/doi/10.1111/nph.15596 by M</p><p>ozam</p><p>bique H</p><p>inari N</p><p>PL</p><p>, W</p><p>iley O</p><p>nline L</p><p>ibrary on [31/08/2024]. See the T</p><p>erm</p><p>s and C</p><p>onditions (https://onlinelibrary.w</p><p>iley.com</p><p>/term</p><p>s-and-conditions) on W</p><p>iley O</p><p>nline L</p><p>ibrary for rules of use; O</p><p>A</p><p>articles are governed by the applicable C</p><p>reative C</p><p>om</p><p>m</p><p>ons L</p><p>icense</p><p>Our current understanding of the nature of plant–microbe</p><p>associations and the diversity of pathogens in plants is extremely</p><p>patchy. Discovery of pathogens associated with plants has been</p><p>highly biased to plants of agricultural importance (usually</p><p>angiosperms). Little is known about pathogens in algae and</p><p>nonflowering land plants. With the help of metagenomic</p><p>approaches, further exploring the diversity of microbes associated</p><p>with plants might provide important insights into the pathogen</p><p>spectrum for plants as well as the origin and evolution of plant–</p><p>pathogen interactions.</p><p>Although it is difficult to reveal the nature of the ancient plant–</p><p>microbe associations, it is safe to conclude that many of these</p><p>associations are/were antagonistic (Upson et al., 2018), as exempli-</p><p>fied by numerous plant pathogens known to date. It seems inevitable</p><p>that some early plants evolved strategies (as aforementioned) to fight</p><p>against microbial infections. With the recent development of next-</p><p>generation sequencing, genomes and transcriptomes of more and</p><p>more plants have been sequenced. Comparative analyses of plant</p><p>genome-scale data will help us to address some central questions,</p><p>such as: (1) When did different plant immune strategies originate?</p><p>(2) How did plant immunity-related genes evolve?</p><p>III. Evolutionary dynamics of plant–pathogen</p><p>interactions</p><p>Pathogens infect plants, causing reduced fitness and mortality.</p><p>The conflicts between plants and pathogens result in perpetual</p><p>coevolutionary cycles, which are often known as ‘Red Queen’</p><p>dynamics (Van Valen, 1973; Brockhurst et al., 2014; Sironi</p><p>et al., 2015). Red Queen dynamics can be broadly divided into</p><p>three broad classes (Brockhurst et al., 2014; Sironi et al., 2015;</p><p>Fig. 3). Fluctuating Red Queen: rare host genotypes in a host</p><p>population have higher fitness than common genotypes because</p><p>pathogens preferentially attack common genotypes, a</p><p>phenomenon known as negative frequency-dependent selection.</p><p>Negative frequency-dependent selection drives allele frequency</p><p>fluctuating in both host and pathogen populations, thus</p><p>maintaining genetic variation within them. Diverse ecological</p><p>and epidemiological factors could cause negative frequency-</p><p>dependent selection on host resistance and pathogen virulence</p><p>(see Brown & Tellier, 2011, for a detailed review). Escalatory</p><p>Red Queen: hosts and pathogens undergo rounds of arms race,</p><p>that is hosts are under selection to eliminate pathogens, while</p><p>pathogens evolve to evade host immunity. Chase Red Queen:</p><p>directional selection drives evolutionary chases between hosts</p><p>and pathogens, that is hosts are under selection to reduce the</p><p>level of interaction with pathogens, while pathogens undergo</p><p>selection to strengthen their interactions with hosts. Both</p><p>Escalatory and Chase Red Queen scenarios result in cycling</p><p>selective sweeps and are essentially different forms of arms race</p><p>dynamics. Empirical studies based on single natural populations</p><p>or microbial organisms in the laboratory have revealed that both</p><p>frequency-dependent selection and arms race dynamics poten-</p><p>tially drive coevolutionary processes between hosts and</p><p>pathogens (Chaboudez & Burdon, 1995; Thrall et al., 2012;</p><p>Betts et al., 2014).</p><p>The situation becomes more</p><p>complex in nature, because</p><p>some sort of biogeographical structure exists almost universally</p><p>in both plant and pathogen species (Green et al., 2008; Peay</p><p>et al., 2016). The development of metapopulation theory</p><p>(Levins, 1969; Hanski, 1999) and the geographical mosaic</p><p>theory of coevolution (Thompson, 1999, 2005) highlights the</p><p>importance of spatio-temporal heterogeneity in shaping coevo-</p><p>lutionary processes. Indeed, plant disease incidence and severity</p><p>display spatial and temporal variation at the local population</p><p>level (Burdon & Thrall, 2014). Clearly, plant–pathogen</p><p>interactions do not proceed as a unit but vary in space and</p><p>over time (Thompson, 1999, 2005; Burdon & Thrall, 2014).</p><p>Pathogens may infect some local populations but not all</p><p>populations of a species across geographic ranges. The outcomes</p><p>of plant–pathogen interactions may vary among local popula-</p><p>tions and over time (Thompson, 1999, 2005). This spatially</p><p>and temporally varying selection might maintain genetic</p><p>variations across different local plant and pathogen populations</p><p>(Gillespie, 1998; Gloss et al., 2016).</p><p>IV. Evolutionary signature of plant–pathogen</p><p>interactions</p><p>How do coevolutionary processes influence the evolution of host</p><p>immunity at the molecular level? Frequency-dependent selection</p><p>and arms race dynamics are expected to result in different patterns</p><p>of polymorphisms (Woolhouse et al., 2002). Negative frequency-</p><p>dependent selection maintains alleles over long periods of time, a</p><p>commonly known form of balancing selection. In general,</p><p>balancing selection refers to the evolutionary processes of main-</p><p>taining genetic variation within species (Charlesworth, 2006).</p><p>Spatially and temporally varying selection and heterozygote</p><p>advantage (negligible for selfing plant species, such as A. thaliana)</p><p>can also generate balancing selection. Arms race dynamics involves</p><p>(a)</p><p>(b)</p><p>Fig. 3 Different scenarios of ‘RedQueen’ dynamics.Different colors indicate</p><p>different host plant genotypes. (a) Fluctuating Red Queen drives allele</p><p>frequency fluctuations and maintains genetic variation in the host</p><p>population. (b) Escalatory or Chase Red Queen results in recurrent selective</p><p>sweeps in host plant populations.</p><p>New Phytologist (2019) 222: 70–83 � 2018 The Author</p><p>New Phytologist� 2018 New Phytologist Trustwww.newphytologist.com</p><p>Review Tansley review</p><p>New</p><p>Phytologist74</p><p>14698137, 2019, 1, D</p><p>ow</p><p>nloaded from</p><p>https://nph.onlinelibrary.w</p><p>iley.com</p><p>/doi/10.1111/nph.15596 by M</p><p>ozam</p><p>bique H</p><p>inari N</p><p>PL</p><p>, W</p><p>iley O</p><p>nline L</p><p>ibrary on [31/08/2024]. See the T</p><p>erm</p><p>s and C</p><p>onditions (https://onlinelibrary.w</p><p>iley.com</p><p>/term</p><p>s-and-conditions) on W</p><p>iley O</p><p>nline L</p><p>ibrary for rules of use; O</p><p>A</p><p>articles are governed by the applicable C</p><p>reative C</p><p>om</p><p>m</p><p>ons L</p><p>icense</p><p>cyclical fixation of alleles in both host and pathogen populations,</p><p>creating recurrent selective sweeps, which reduces genetic variation</p><p>at both selected loci and nearby loci. Various statistical approaches</p><p>have been developed to identify selection and distinguish different</p><p>forms of selection (reviewed by Nielsen, 2005; Vitti et al., 2013).</p><p>Comparative approaches involving multiple species are often</p><p>used to identify selection events occurring in the deep past,</p><p>reflecting macroevolutionary trends between, rather than within,</p><p>species (Nielsen, 2005; Vitti et al., 2013). One commonly used</p><p>statistic is to compare nonsynonymous (dN) and synonymous (dS)</p><p>substitution rates (Yang & Bielawski, 2000; Nielsen, 2005;</p><p>Daugherty & Malik, 2012; Sironi et al., 2015). A dN : dS ratio</p><p>significantly > 1 provides strong evidence for positive selection,</p><p>while dN : dS ratios ≤ 1 indicate purifying (negative) selection</p><p>against deleteriousmutation.However, the dN : dS statistic appears</p><p>to be very conservative, because: a gene might undergo purifying</p><p>selection for most of the time and occasionally evolve under</p><p>episodic adaptive change (Yang&Bielawski, 2000;Nielsen, 2005);</p><p>and many sites are under strong purifying selection due to</p><p>functional constraints, and positive selection acts only on a small</p><p>proportion of sites (Murrell et al., 2012). To address these</p><p>problems, various methods have been developed to detect specific</p><p>lineages in a phylogeny or individual sites in a gene subject to</p><p>episodic positive selection (Yang & Bielawski, 2000; Murrell et al.,</p><p>2012).</p><p>Population genetic methods have been used to identify ongoing</p><p>selection events within species, reflecting microevolutionary trends</p><p>(Vitti et al., 2013). Within a population, while positive selection</p><p>drives a beneficial allele to reach high frequency or fixation and</p><p>causes reduced genetic variation, balancing selection maintains</p><p>genetic variation. Various methods have been developed to</p><p>distinguish different forms of selection occurring within a popu-</p><p>lation, which are based on allele frequency spectrum, linkage</p><p>disequilibrium or population differentiation (Nielsen, 2005; Vitti</p><p>et al., 2013). A commonly used test is Tajima’sD, which compares</p><p>the average number of pairwise differences between individuals</p><p>with the total number of segregating sites within population</p><p>(Tajima, 1989). A selective sweep creates an excess of rare alleles,</p><p>while balancing selection maintains alleles of intermediate fre-</p><p>quency. The rare alleles contribute less to pairwise differences</p><p>between individuals than alleles of intermediate frequency. There-</p><p>fore, negative and positive values of D may indicate positive</p><p>selection and balancing selection, respectively. Note that Tajima’s</p><p>D is sensitive to demographic events; population contraction and</p><p>population expansion can also result in positive and negative D</p><p>values. Selective and demographic events could be distinguished by</p><p>comparing locus-specific data with genome-wide data, because</p><p>demographic processes influence the whole genome (Vitti et al.,</p><p>2013). Some population genetic methods for detecting selection</p><p>are also based on comparing levels of polymorphism within and</p><p>divergence between species, such as the McDonald–Kreitman test</p><p>(McDonald & Kreitman, 1991) and Hudson–Kreitman–Aguade</p><p>(HKA) test (Hudson et al., 1987).</p><p>With the accumulation of sequences at both the species and</p><p>population level, comparative analyses or population genetic</p><p>methods have been extensively used to elucidate the selection</p><p>pressures underlying the evolution of immunity related genes</p><p>(discussed below).</p><p>V. Origin and evolution of RLK proteins</p><p>The protein kinase superfamily is widely present in all the three</p><p>domains of life (Leonard et al., 1998). In eukaryotes, protein</p><p>kinases are among the largest protein families usually with</p><p>hundreds to thousands of copies (Lehti-Shiu & Shiu, 2012).</p><p>Although RLKs are a group of proteins defined structurally by the</p><p>presence of an extracellular ligand-binding domain, a single-pass</p><p>transmembrane domain and an intracellular kinase domain</p><p>(Fig. 2), RLKs and RLCKs cluster together within the superfamily</p><p>of eukaryotic serine/threonine/tyrosine kinases based on phyloge-</p><p>netic analyses of the kinase domain (Shiu & Bleecker, 2001). Plant</p><p>RLKs and RLCKs belong to the RLK/Pelle family, because plant</p><p>RLKs are closely related to Drosophila Pelle proteins and animal</p><p>cytoplasmic kinases (Shiu & Bleecker, 2001). RLCKs themselves</p><p>do not form a single independent cluster and were embedded</p><p>within the diversity of RLKs, indicating they might have arisen</p><p>multiple times from RLKs through deleting an extracellular</p><p>domain (and transmembrane domain) and/or theymight represent</p><p>ancestral forms from which RLKs originated (Shiu & Bleecker,</p><p>2001).</p><p>While the RLK/Pelle family is present in the genomes of plants,</p><p>animals and Plasmodium, it is not present in fungal genomes (Shiu</p><p>& Bleecker, 2003). It was proposed that the RLK/Pelle family</p><p>originated before the divergence of plants and animals but was lost</p><p>in fungal lineages after the split of fungi and animals (Shiu &</p><p>Bleecker, 2001, 2003). Because the animal RLK/Pelle proteins do</p><p>not cluster together (Shiu & Bleecker, 2003), it is still possible that</p><p>animal RLK/Pelle proteins originated by multiple horizontal gene</p><p>transfers</p><p>(note that the occurrence and rate of horizontal gene</p><p>transfer is controversial (Martin, 2017; Leger et al., 2018)). The</p><p>deep history of the RLK/Pelle family appears to be more complex</p><p>than previously thought. Further phylogenetic analyses are needed</p><p>to evaluate different hypotheses.</p><p>Within plants, RLKs are present in charophytes and land plants</p><p>(Fig. 4; Sasaki et al., 2007; Delaux et al., 2015). Although RLK/</p><p>Pelle kinase members have been identified in some, but not all,</p><p>chlorophytes (Lehti-Shiu et al., 2009; Liu et al., 2017), the known</p><p>RLK/Pelle proteins in chlorophytes lack any extracellular domain</p><p>(Lehti-Shiu et al., 2009). Canonical RLKs with extracellular</p><p>domains, such as LRR and LysM domains, have been identified</p><p>in charophytes (Sasaki et al., 2007; Delaux et al., 2015; Bowman</p><p>et al., 2017; Nishiyama et al., 2018). The most parsimonious</p><p>explanation is that canonical RLK architecture originated before</p><p>the divergence of land plants from charophytes, but after the</p><p>divergence of charophytes and chlorophytes. However, several</p><p>questions remain: Are there RLKs in other charophytes? To date,</p><p>only two charophyte genomes have been sequenced. Analyzing</p><p>more charophyte genomes will narrow down the time range of RL</p><p>K origin. How did RLKs originate in charophytes? Are there</p><p>RLCKs basal to all the plant RLKs present in charophytes? Since</p><p>RLKs regulate a diverse range of biological processes, from plant</p><p>growth and development to plant–pathogen interactions (Shiu</p><p>� 2018 The Author</p><p>New Phytologist� 2018 New Phytologist Trust</p><p>New Phytologist (2019) 222: 70–83</p><p>www.newphytologist.com</p><p>New</p><p>Phytologist Tansley review Review 75</p><p>14698137, 2019, 1, D</p><p>ow</p><p>nloaded from</p><p>https://nph.onlinelibrary.w</p><p>iley.com</p><p>/doi/10.1111/nph.15596 by M</p><p>ozam</p><p>bique H</p><p>inari N</p><p>PL</p><p>, W</p><p>iley O</p><p>nline L</p><p>ibrary on [31/08/2024]. See the T</p><p>erm</p><p>s and C</p><p>onditions (https://onlinelibrary.w</p><p>iley.com</p><p>/term</p><p>s-and-conditions) on W</p><p>iley O</p><p>nline L</p><p>ibrary for rules of use; O</p><p>A</p><p>articles are governed by the applicable C</p><p>reative C</p><p>om</p><p>m</p><p>ons L</p><p>icense</p><p>et al., 2004), what are the functions of ancestral RLKs? An RLK</p><p>with a malectin-like carbohydrate-binding domain functions as a</p><p>cell-wall sensor and might regulate sexual reproduction in the</p><p>charophyte Closterium peracerosum–strigosum–littorale complex</p><p>(Hirano et al., 2015). Because a majority of LRR-RLKs may be</p><p>PRRs (Boller & Felix, 2009), we infer some, if not all, LRR-RLKs</p><p>in charophytes might serve as PRRs. Sequencing more charophyte</p><p>genomes and functional characterization of RLKs in charophytes</p><p>might further illuminate the origin of RLKs.</p><p>While charophyte genomes contain 20–30 LRR-RLKs, the</p><p>liverwort Marchantia polymorpha genome has at least 107 genes</p><p>with both LRR and kinase domains (Bowman et al., 2017). The</p><p>genomes of land plants have long been known to encode a large</p><p>repertoire of RLK/Pelle proteins (> 320 in Physcomitrella patens,</p><p>> 600 in A. thaliana and > 1100 inOryza sativa) (Shiu & Bleecker,</p><p>2003; Shiu et al., 2004). Expansion and diversification of the RLK/</p><p>Pelle family seem to coincidewith colonization of the landby plants</p><p>(Lehti-Shiu et al., 2009; Bowman et al., 2017). Expansion of the</p><p>RLK/Pelle family was through both tandem duplication and</p><p>segmental/whole genome duplication (Shiu & Bleecker, 2003;</p><p>Shiu et al., 2004). Duplicate RLKs provide ‘free’ copies for novel</p><p>MAMP recognition.Comparison of paralogous genes revealsmany</p><p>RLK groups have a dN : dS > 1 (Shiu et al., 2004; Fischer et al.,</p><p>2016). Note that dN : dS > 1 for a pair of genes indicates a net</p><p>acceleration of protein evolution (Lynch & Conery, 2000). The</p><p>sites under accelerated evolution are mainly distributed in the</p><p>extracellular domains (Shiu et al., 2004; Fischer et al., 2016),</p><p>suggesting the extracellular domains might diversify to recognize</p><p>novel MAMP alleles or types. While the RLK/Pelle genes that</p><p>function in plant growth and development have rarely undergone</p><p>gene duplication, expansion of the RLK/Pelle family is suggested to</p><p>have mainly involved genes related to biotic defense responses in</p><p>plants (Shiu et al., 2004; Lehti-Shiu et al., 2009).</p><p>Members of the plant RLK/Pelle family vary greatly in their</p><p>extracellular domains, most of which are LRR domains (Shiu &</p><p>Bleecker, 2001, 2003). More than 10 domain types have been</p><p>found to be associated with the plant RLK/Pelle family (Lehti-Shiu</p><p>et al., 2009).With a few exceptions, RLKswith similar extracellular</p><p>domains tend to cluster together and can be classified into</p><p>subfamilies (Shiu & Bleecker, 2003). However, a protein might</p><p>have a domain organization different from that of the majority of</p><p>the subfamily, indicating potential domain gain events have</p><p>Arabidopsis thaliana</p><p>Oryza sativa</p><p>Picea abies</p><p>Selaginella moellendorffii</p><p>Physcomitrella patens</p><p>Marchantia polymorpha</p><p>Cyanophora paradoxa</p><p>Chondrus crispus</p><p>Cyanidioschyzon merolae</p><p>Galdieria sulphuraria</p><p>Chlamydomonas reinhardtii</p><p>Coccomyxa subellipsoidea</p><p>Ostreococcus lucimarinus</p><p>Chara braunii</p><p>Klebsormidium nitens</p><p>Origin of</p><p>seed plants</p><p>+miR482/2118</p><p>+NPR</p><p>Origin of</p><p>land plants</p><p>+RLK</p><p>+NLR</p><p>?</p><p>+RNAi</p><p>Origin of</p><p>plants</p><p>Land plants</p><p>Charophyta</p><p>Chlorophyta</p><p>Rhodophyta</p><p>Glaucophyta</p><p>RLK NLR NPR DCL AGO</p><p>Fig. 4 The origin anddistribution of key components of the plant immune system. The phylogenetic relationship of plant species is based on Blanc et al. (2012),</p><p>Bowman et al. (2017), Nishiyama et al. (2018) and Betts et al. (2018). To identify the presence of homologs of plant immune-related proteins within</p><p>representative plant genomes, the BLASTP algorithm was employed with an e cut-off value of 10�5. Arabidopsis thaliana proteins were used as queries: the</p><p>kinasedomainofRLK,AT5G46330; theNB-ARCdomainofNLR,AT1G12220;NPR1,AT1G64280;DCL1,AT1G01040; andAGO1,AT1G48410.Opencircles</p><p>represent no significant hits. Gray circles indicate homologs are present within the related genome, but the homologs do not encode canonical domain</p><p>architectures: an extracellular domain, a transmembrane domain and an intracellular kinase domain for RLKs; an NB-ARC domain and LRRs for NLRs; BTB,</p><p>Ank_2andNPR1-like_C forNPRs; andDEAD, helicase, ribonuclease III, anddouble-strandedRNAbindingmotif forDCLs. Filled circles indicate the presenceof</p><p>proteinswith canonical domain architectures. The domain architectureswere annotatedusing SMART (http://smart.embl.de) andCD-SEARCH (https://www.ncb</p><p>i.nlm.nih.gov/Structure/cdd/wrpsb.cgi). Shao et al. (2018) recently identified the presence of NLR genes in two chlorophytes. However, the possibility</p><p>thatNLR genes originated in the common ancestor of green plants requires many independent losses of NLRs in chlorophytes, which seems unlikely, and the</p><p>possibility that chlorophyteNLR genes originated fromhorizontal gene transfer or sequencing error cannot be formally excluded.We therefore label the origin</p><p>of NLR genes with a question mark.</p><p>New Phytologist (2019) 222: 70–83 � 2018 The Author</p><p>New Phytologist� 2018 New Phytologist Trustwww.newphytologist.com</p><p>Review Tansley review</p><p>New</p><p>Phytologist76</p><p>14698137, 2019, 1, D</p><p>ow</p><p>nloaded from</p><p>https://nph.onlinelibrary.w</p><p>iley.com</p><p>/doi/10.1111/nph.15596 by M</p><p>ozam</p><p>bique H</p><p>inari N</p><p>PL</p><p>, W</p><p>iley O</p><p>nline L</p><p>ibrary on [31/08/2024]. See the T</p><p>erm</p><p>s and C</p><p>onditions (https://onlinelibrary.w</p><p>iley.com</p><p>/term</p><p>s-and-conditions) on W</p><p>iley O</p><p>nline L</p><p>ibrary for rules of use; O</p><p>A</p><p>articles are governed by the applicable C</p><p>reative C</p><p>om</p><p>m</p><p>ons L</p><p>icense</p><p>https://www.ncbi.nlm.nih.gov/Structure/cdd/wrpsb.cgi</p><p>https://www.ncbi.nlm.nih.gov/Structure/cdd/wrpsb.cgi</p><p>occurred (Lehti-Shiu et al., 2009). The domains gained are usually</p><p>old ones that are found in other RLK subfamilies (Shiu&Bleecker,</p><p>2003; Lehti-Shiu et al., 2009). Innovation to RLK domain</p><p>architectures occurred throughout land plant lineages (Lehti-Shiu</p><p>et al., 2009). Moreover, as already mentioned, RLCKs usually fall</p><p>within the diversity of RLKs, indicating frequent losses of</p><p>extracellular domains also occurred. Taken together, domain</p><p>shuffling and molecular tinkering appear to play an important role</p><p>in the evolution</p><p>of RLK structures (Lehti-Shiu et al., 2009).</p><p>The MAMP perception systems are sometimes conserved, but</p><p>more often restricted within smaller plant taxonomic groups (e.g.</p><p>species, genus and family) (Boller & Felix, 2009). The bacterial</p><p>flagellin was perceived by FLAGELLIN-SENSING 2 (FLS2) by</p><p>direct binding of a 22-amnio-acid stretch of the N-terminus of</p><p>bacterial flagellin (referred to as flg22) (Chinchilla et al., 2006;</p><p>Zipfel, 2014). Perception of flg22 appears to occur in all the major</p><p>lineages of seed plants (Boller & Felix, 2009; Albert et al., 2010).</p><p>Moreover, functional FLS2 orthologs have been characterized in</p><p>A. thaliana, tobacco (Nicotiana benthamiana), tomato (Solanum</p><p>lycopersicum), grapevine (Vitis vinifera) and O. sativa (Hann &</p><p>Rathjen, 2007; Robatzek et al., 2007; Takai et al., 2008; Trda et al.,</p><p>2014; Zipfel, 2014). It follows that the perception of flg22 by FLS2</p><p>arose earlier than the origin of angiosperms. The elongation factor</p><p>Tu (EF-Tu) represents another well-characterized MAMP. The</p><p>first 18 amino acids of EF-Tu (elf18) are directly recognized by the</p><p>EF-Tu receptor (EFR) (Zipfel, 2014). Responsiveness to EF-Tu</p><p>peptides seems to be restricted within the species of the family</p><p>Brassicaceae, suggesting a more recent origin of this interaction</p><p>(Kunze et al., 2004). Therefore, the recognition of MAMP by</p><p>RLKs seems to be evolutionarily dynamic.</p><p>In general, MAMPs evolve slowly (Jones &Dangl, 2006). PRRs</p><p>are thus expected to evolve under purifying selection to maintain</p><p>their affinity to MAMPs and thus their ability to detect microbes</p><p>(Vetter et al., 2012). Indeed, analyses of orthologous LRR-RLK</p><p>genes in angiosperms suggest the majority of LRR-RLK genes</p><p>underwent purifying selection over long time scales (Fischer et al.,</p><p>2016). However, variation has been observed in some MAMPs,</p><p>such as flg22 and flgII-28 (a distinct MAMP within flagellin),</p><p>within species, and different MAMP alleles induce different</p><p>immune responses (Cai et al., 2011;Clarke et al., 2013). Binding to</p><p>MAMPs might be highly variable among different genotypes</p><p>within species and across different species (Vetter et al., 2012).</p><p>Under this scenario, PRRs could evolve to enhance their affinity to</p><p>MAMP alleles with which they interact and thus may display some</p><p>signature of selection (positive or balancing selection). Analysis of</p><p>the variation pattern of the 50 region (noncoding region and the N-</p><p>terminus of extracellular domain) of the FLS2 locus within</p><p>A. thaliana indicates this region underwent positive selection</p><p>(Vetter et al., 2012). A genome-wide analysis of different</p><p>A. thaliana accessions suggests some RLK genes were indeed under</p><p>positive or balancing selection (Borevitz et al., 2007).</p><p>The evolutionary scenarios become more complicated, when</p><p>some RLPs, such as the tomato Cf-2 protein, do not directly</p><p>recognize MAMPs but monitor the host target of the pathogen</p><p>effector (Rooney et al., 2005). The fungal protease inhibitor AVR2</p><p>directly interacts with and inhibits paralogous secreted cysteine</p><p>proteases of Rcr3 and Pip1 in tomato (Rooney et al., 2005; Shabab</p><p>et al., 2008; Ilyas et al., 2015). Cf-2 confers resistance to the leaf</p><p>mold pathogenCladosporium fulvum by detecting themodification</p><p>ofRcr3 induced byAVR2 (Rooney et al., 2005). In thismultiplayer</p><p>antagonistic system, different components might evolve under</p><p>contrasting evolutionary forces (van derHoorn&Kamoun, 2008).</p><p>Evolution of the Rcr3 gene is characterized by gene duplication,</p><p>frequent gene conversion and balancing selection in the wild</p><p>tomato species Solanum peruvianum (Horger et al., 2012). Popu-</p><p>lation genetic analyses suggest a potential role of balancing selection</p><p>in shaping the diversity at the 50 end of the Cf-2 gene in the wild</p><p>tomato species Solanum pimpinellifolium (Caicedo & Schaal,</p><p>2004).</p><p>A limited number of studies available to date indicate that RLKs</p><p>underwent purifying selection over long time scales, and some RLK</p><p>genes did undergo positive selection and balancing selection at the</p><p>population level. However, to what extent RLK genes underwent</p><p>different forms of selection remains unknown. Most population</p><p>genetic studies are based on a model species or its wild relatives.</p><p>Therefore, more comparative genomic and population genetic</p><p>analyses, especially in charophytes and nonflowering land plants,</p><p>are needed to fully understand the long-term and short-term</p><p>evolutionary dynamics of RLK genes.</p><p>VI. Origin and evolution of NLR proteins</p><p>AnNLR protein usually contains anN-terminal signaling domain,</p><p>a nucleotide-binding adaptor shared by APAF-1, certain R gene</p><p>products and CED-4 (NB-ARC) domain, and a series of LRRs</p><p>(Urbach & Ausubel, 2017). The NB-ARC domain belongs to the</p><p>signal transduction ATPases with numerous domains (STAND)</p><p>superfamily. Animal innate immunity involvesNod-like receptors,</p><p>which also contain a STAND domain known as NACHT (NAIP,</p><p>CIIA, HET-E and TEP1) and a series of LRRs (Ausubel, 2005).</p><p>Phylogenetic analyses reveal that the similarity of domain organi-</p><p>zation between plant NLRs and animal Nod-like receptors arose</p><p>through convergent evolution, rather than having a commonorigin</p><p>(Urbach&Ausubel, 2017).Comparative genomic analysis of plant</p><p>species that represent all the major plant lineages suggests that</p><p>NLRs are widely distributed in charophytes and land plants, but</p><p>not rhodophytes or glaucophytes (Fig. 4; Gao et al., 2018).</p><p>Interestingly, a recent study found the presence of NLR genes in</p><p>two out of 24 chlorophyte species (Shao et al., 2018). However,</p><p>given the scattered distribution ofNLRs in chlorophyte species, the</p><p>possibility that these NLR genes originated through horizontal</p><p>gene transfer or were generated by sequencing error or contami-</p><p>nation remains to be formally excluded. Nevertheless, the distri-</p><p>bution of NLRs in plants suggests that NLRs originated before the</p><p>divergence between charophytes and land plants, possibly in the</p><p>commonancestor of greenplants (Gao et al., 2018;Shao et al., 2018).</p><p>Plant NLR proteins are traditionally classified into two types</p><p>based on the presence or absence of the Toll/interleukin-1 receptor</p><p>(TIR) domain at the N-terminus, that is TIR-NBS-LRR (TNL)</p><p>and non-TIR-NBS-LRR (nTNL) proteins (McHale et al., 2006;</p><p>Shao et al., 2016). Many nTNLs contain a coiled-coil motif at the</p><p>N-terminus, and are thus referred to as CC-NBS-LRRs (CNLs).</p><p>� 2018 The Author</p><p>New Phytologist� 2018 New Phytologist Trust</p><p>New Phytologist (2019) 222: 70–83</p><p>www.newphytologist.com</p><p>New</p><p>Phytologist Tansley review Review 77</p><p>14698137, 2019, 1, D</p><p>ow</p><p>nloaded from</p><p>https://nph.onlinelibrary.w</p><p>iley.com</p><p>/doi/10.1111/nph.15596 by M</p><p>ozam</p><p>bique H</p><p>inari N</p><p>PL</p><p>, W</p><p>iley O</p><p>nline L</p><p>ibrary on [31/08/2024]. See the T</p><p>erm</p><p>s and C</p><p>onditions (https://onlinelibrary.w</p><p>iley.com</p><p>/term</p><p>s-and-conditions) on W</p><p>iley O</p><p>nline L</p><p>ibrary for rules of use; O</p><p>A</p><p>articles are governed by the applicable C</p><p>reative C</p><p>om</p><p>m</p><p>ons L</p><p>icense</p><p>Some nTNLs possess resistance to the powdery mildew8 (RPW8)</p><p>domain, and are referred to as RPW8-NBS-LRRs (RNLs) (Xiao</p><p>et al., 2001). Both TNLs and nTNLs are present in charophytes</p><p>and chlorophytes, suggesting NLR genes have diversified before</p><p>the emergence of land plants, possibly in the common ancestor of</p><p>green plants (Gao et al., 2018; Shao et al., 2018). For TNLs,</p><p>nTNLs or RNLs, none forms a monophyletic group (Gao et al.,</p><p>2018). Domain gain and loss occurred frequently in the evolution</p><p>of NLRs (Gao et al., 2018). TNLs and RNLs appear to have</p><p>originated independently through gain of TIR or RPW8 domains,</p><p>respectively (Gao et al., 2018). In addition to TIR and RPW8</p><p>domains, NLRs are also associated with other domains, such as</p><p>Pkinase and DUF676 (Xue et al., 2012; Gao et al., 2018). NLR</p><p>proteins have been found to be fused with other noncanonical</p><p>domains (known as integrated domains); for example, NLR</p><p>proteins, A. thaliana RRS1 and O. sativa RGA5, carry a WRKY</p><p>transcription factor domain and a heavy metal-associated (HMA)</p><p>domain, respectively (Le Roux et al., 2015; Sarris et al., 2015). The</p><p>integrated domains have been proposed</p><p>to serve as ‘baits’ for</p><p>pathogen effectors (Kroj et al., 2016; Sarris et al., 2016). The</p><p>integration into NLRs appears to be widespread and frequent in</p><p>angiosperms (Kroj et al., 2016; Sarris et al., 2016). It remains to be</p><p>clarified whether integrated domains occurred frequently in NLRs</p><p>of charophytes and nonflowering land plants.</p><p>The repertoire of NLR genes has been shaped jointly by</p><p>duplication, translocation, deletion and promiscuous gene</p><p>exchange events (Bergelson et al., 2001; Meyers et al., 2003; Gao</p><p>et al., 2018). Studies based on comparison of NLR gene</p><p>paralogs have frequently found evidence for adaptive divergence</p><p>(dN : dS > 1), suggesting rapid diversification ofNLR genes within</p><p>species (Bergelson et al., 2001; Mondragon-Palomino et al., 2002;</p><p>Yang et al., 2013;Karasov et al., 2014a;Gao et al., 2018). Positively</p><p>selected sites were located not only in the LRR domain but also</p><p>outside the LRR domain (Mondragon-Palomino et al., 2002; Gao</p><p>et al., 2018). Comparison of orthologous NLR genes suggests</p><p>nonsynonymous substitutions have accumulated more slowly than</p><p>synonymous substitutions (Bergelson et al., 2001; Wang et al.,</p><p>2011). However, it remains possible that some sites or lineages</p><p>underwent episodic positive selection.</p><p>A classic arms race entails cycling selective sweeps and thus causes</p><p>a reduction of diversity at a locus (Bergelson et al., 2001).However,</p><p>selective sweeps occurred only in a small proportion of NLR genes</p><p>(Bergelson et al., 2001).NLR genes are the most polymorphic loci</p><p>in plants and frequently persist as polymorphisms for millions of</p><p>years in nature (Gan et al., 2011; Karasov et al., 2014a,b). Long-</p><p>lived balanced polymorphisms in NLR genes could be either</p><p>presence–absence polymorphisms, where susceptible individuals</p><p>are usually lacking related NLR genes, or nonpresence/absence</p><p>polymorphisms (Karasov et al., 2014b). The best studied NLR</p><p>genes with balanced presence/absence polymorphisms are RPM1,</p><p>which recognizes Pseudomonas pathogens carrying AvrRpm1 or</p><p>AvrB, and RPS5, which recognizes Pseudomonas syringae carrying</p><p>avrPphB (Stahl et al., 1999; Tian et al., 2002; Karasov et al.,</p><p>2014b). The null alleles of RPM1 and RPS5 might be maintained</p><p>by selection due to costs of resistance (Stahl et al., 1999; Tian</p><p>et al., 2003; Karasov et al., 2014b). For nonpresence/absence</p><p>polymorphisms, many NLR gene alleles are also maintained by</p><p>balancing selection, but few loci are under directional selection</p><p>(Rose et al., 2004; Bakker et al., 2006; Karasov et al., 2014b). Rps2</p><p>alleles form two major clades, one resistant and one susceptible to</p><p>Pseudomonas syringae pv. avrRpt2, and the nucleotide diversity</p><p>exhibits a signature of balancing selection (Mauricio et al., 2003;</p><p>MacQueen et al., 2016).Given plantswith resistant and susceptible</p><p>alleles share similar fitness in the absence of disease, the mainte-</p><p>nance of Rps2 polymorphism cannot be explained by costs of</p><p>resistance but might have to involve temporally and spatially</p><p>varying selection (MacQueen et al., 2016). Therefore, the arms race</p><p>model might represent a poor metaphor for the evolutionary</p><p>dynamics of plant NLR genes, and NLR genes evolved mainly by</p><p>balancing selection (Bergelson et al., 2001). Again, this conclusion</p><p>comes mainly from studies of model species. More work is needed</p><p>to explore the evolutionary dynamics of NLR genes in chloro-</p><p>phytes, charophytes and nonflowering land plants.</p><p>There are parallels and differences between RLK and NLR</p><p>evolution. Both RLK and NLR genes duplicated frequently.</p><p>Frequent domain gain and loss occurred during the course of</p><p>RLK and NLR evolution. Comparative studies suggest that many</p><p>paralogous copies experienced adaptive divergence.However,NLR</p><p>proteins are generally more variable than other proteins at both the</p><p>sequence and expression level among different A. thaliana acces-</p><p>sions, while RLK proteins are similar to other proteins (Gan et al.,</p><p>2011). A greater proportion of NLR genes are found to be under</p><p>balancing selection than RLK genes (Borevitz et al., 2007). Several</p><p>possible mechanisms might explain this difference: MAMPs</p><p>evolved slowly and have limited variation, while pathogen effectors</p><p>evolved rapidly and exhibit extensive diversity (Upson et al., 2018);</p><p>and some RLKs function in plant growth and development and</p><p>mainly underwent purifying selection.</p><p>VII. Origin and evolution of SA signaling</p><p>Comparative genomic analyses show all the key components of SA</p><p>signaling are present in land plants, but not in charophytes,</p><p>suggesting that SA signaling might have originated in the last</p><p>common ancestor of land plants (Fig. 4; Wang et al., 2015). In</p><p>A. thaliana,NPR1 andNPR3/4 are SA receptors, but play opposite</p><p>roles in regulating the transcription of SA-induced defense genes</p><p>(Ding et al., 2018). NPR1 and NRP3/4 serve as a transcriptional</p><p>co-activator and transcriptional co-repressors, respectively (Ding</p><p>et al., 2018). Phylogenetic analysis suggests that duplication of the</p><p>NPR1/2 progenitor and the NPR3/4 progenitor occurred before</p><p>the emergence of angiosperms but after the divergence of</p><p>lycophytes and angiosperms (Wang et al., 2015). While the</p><p>liverwort M. polymorpha and the lycophyte Selaginella</p><p>moellendorffii only have one copy of the NPR protein, the moss</p><p>P. patens has two NPR copies that arose through a moss-specific</p><p>duplication event (Wang et al., 2015). It seems that SA signaling</p><p>evolved to be complex independently in different land plant</p><p>lineages. SA is detected in the charophyte Klebsormidium nitens</p><p>(Hori et al., 2014). Indeed, most genes involved in the phenyl-</p><p>propanoid pathway, one of the two routes for SA biosynthesis, are</p><p>present in charophytes (Shine et al., 2016; J. de Vries et al., 2017;</p><p>New Phytologist (2019) 222: 70–83 � 2018 The Author</p><p>New Phytologist� 2018 New Phytologist Trustwww.newphytologist.com</p><p>Review Tansley review</p><p>New</p><p>Phytologist78</p><p>14698137, 2019, 1, D</p><p>ow</p><p>nloaded from</p><p>https://nph.onlinelibrary.w</p><p>iley.com</p><p>/doi/10.1111/nph.15596 by M</p><p>ozam</p><p>bique H</p><p>inari N</p><p>PL</p><p>, W</p><p>iley O</p><p>nline L</p><p>ibrary on [31/08/2024]. See the T</p><p>erm</p><p>s and C</p><p>onditions (https://onlinelibrary.w</p><p>iley.com</p><p>/term</p><p>s-and-conditions) on W</p><p>iley O</p><p>nline L</p><p>ibrary for rules of use; O</p><p>A</p><p>articles are governed by the applicable C</p><p>reative C</p><p>om</p><p>m</p><p>ons L</p><p>icense</p><p>S. de Vries et al., 2017). NPR homologs can be found in some</p><p>charophyte species, but they do not encode all the domains that</p><p>NPRs contain (Wang et al., 2015; Fig. 4). Functional analyses of</p><p>NPR homologs in charophytes and nonflowering land plants could</p><p>help us further understand the origin, evolution andmechanisms of</p><p>SA signaling.</p><p>VIII. Origin and evolution of RNA-based defense</p><p>Dicer and AGO proteins are present throughout eukaryotes, and a</p><p>functional RNAi system is likely to pre-date the last common</p><p>ancestor of the extant eukaryotes (Shabalina & Koonin, 2008;</p><p>Mukherjee et al., 2013). DCL and AGO proteins are ubiquitously</p><p>present in plants, but are absent in some rhodophytes (such as</p><p>Cyanidioschyzon merolae) and some chlorophytes (such as</p><p>Ostreococcus tauri and O. lucimarinus) (Fig. 4), indicating that</p><p>RNAi is not essential in all eukaryotes, especially unicellular</p><p>organisms (Shabalina & Koonin, 2008; Cerutti et al., 2011). Four</p><p>distinct DCL groups (DCL-1 toDCL-4) seem to have arisen in the</p><p>early evolution of land plants (Mukherjee et al., 2013; Jia et al.,</p><p>2017). Recurrent positive selection occurred in DCL proteins</p><p>throughout plants, especially in DCL-4 proteins that mainly</p><p>mediate antiviral RNA silencing in plants (Mukherjee et al., 2013;</p><p>Jia et al., 2017). Ancestral sequence resurrection suggests that the</p><p>ancestral plant DCL protein exhibits affinity for viral RNA (Jia</p><p>et al., 2017). The affinity for viral RNA was increased during the</p><p>evolution of DCL-4 proteins and was increased and then decreased</p><p>during the evolution of DCL-2s (Jia et al., 2017). Indeed, antiviral</p><p>RNA silencing is mediated by DCL-4 and probably DCL-2 in</p><p>some conditions (Ding, 2010). In algae, while RNAi has been</p><p>suggested to be involved in repressing transposons, its role in</p><p>antiviral immunity remains to be explored (Cerutti et al., 2011).</p><p>In plants, microRNAs (miRNAs), a class of c. 21-nucleotide-</p><p>long small RNAs, regulate stress responses and development. As</p><p>NLRs are associated with fitness costs (Stahl et al., 1999; Tian et al.,</p><p>2003; Karasov et al., 2014b) and high expression of NLR genes</p><p>might cause phenotypic abnormalities (Stokes et al., 2002), the</p><p>copy number and expression level of NLR genes should be tightly</p><p>controlled. NLR genes are targeted by many miRNA families</p><p>(Shivaprasad et al., 2012; Xia et al., 2015; Zhang et al., 2016).</p><p>Regulation of NLR genes by miRNAs contributes to plant</p><p>immunity to pathogens (Ouyang et al., 2014; de Vries et al.,</p><p>2018b). miRNAs seem to preferentially target highly duplicated</p><p>NLR genes (de Vries et al., 2015, 2018a,b; Zhang et al., 2016).</p><p>Most miRNA families targeting NLR genes appear to be present</p><p>only in specific lineages, suggesting recurrent de novo generation of</p><p>miRNAs targeting NLR genes (Zhang et al., 2016). However, the</p><p>miR482/2118 family is exceptional in its ancient origin. The</p><p>miR482/2118 family targets the NB-ARC domain of NLRs and</p><p>triggers the production of phased secondary siRNAs (phasiRNAs)</p><p>in eudicots, while it triggers the production of phasiRNAs from</p><p>noncoding transcripts in reproductive tissues in monocots</p><p>(Shivaprasad et al., 2012; Xia et al., 2015). In gymnosperms,</p><p>miR482/2118 targets both NLR genes and nocoding RNAs (Xia</p><p>et al., 2015). The miR482/2118 family is absent in mosses and</p><p>lycopods (de Vries et al., 2015). It follows that the interaction</p><p>between NLR genes and miR482/2118 might have originated at</p><p>least in the common ancestor of angiosperms and gymnosperms,</p><p>that is, the early seed plants (Zhang et al., 2016). To keep pace with</p><p>NLR genes that duplicated frequently and evolved rapidly,</p><p>miRNAs evolve at an elevated rate and are highly variable (de</p><p>Vries et al., 2015; Zhang et al., 2016). Without involving complex</p><p>evolution of cis-regulation sequences, birth of novel miRNAs</p><p>represents an economic and efficient way to regulate the diversi-</p><p>fication of NLR genes (Zhang et al., 2016).</p><p>In plants, RNA silencing functions in defense against viruses by</p><p>degrading viral RNA. In turn, viruses evolved diverse viral</p><p>suppressors to avoid RNA silencing (Pumplin & Voinnet, 2013).</p><p>Suppressors of RNA silencing have also been identified in other</p><p>pathogens, such as bacteria and oomycetes (Navarro et al., 2008;</p><p>Pumplin&Voinnet, 2013; J. de Vries et al., 2017; S. de Vries et al.,</p><p>2017). Counter-counter-defense also occurs in host plants</p><p>(Pumplin & Voinnet, 2013). For example, silencing suppression</p><p>of pathogens interferes with expression of theMIR482 gene, results</p><p>in accumulation of NLRs and thus increases plant defense</p><p>(Pumplin & Voinnet, 2013). We still know little about the role</p><p>of RNA silencing in regulating defense in algae and nonflowering</p><p>land plants, which is important for our understanding of the</p><p>complex evolution of RNA silencing network in defense.</p><p>IX. Perspectives</p><p>Plants have been engaged in antagonistic associations with</p><p>microbes for hundreds of millions of years. Defense, counter-</p><p>defense and counter-counter-defense recurrently occur in the</p><p>battlefield between plants and pathogens (Pumplin & Voinnet,</p><p>2013). It is surprising to find that the two tiers of the innate</p><p>immune system have a young origin relative to the history of plants;</p><p>RLK proteins originated in charophytes, and NLR proteins</p><p>originated at least in charophytes, possibly in the common ancestor</p><p>of green plants (Fig. 4). There seems to be an evolutionary ‘big</p><p>bang’ for innate immunity in green algae. It is unclear whether</p><p>RLKs and NLRs are present in other charophytes, such as</p><p>Mesostigmatophyceae and Chlorokybophyceae, due to lack of</p><p>genome-scale data. Conquering terrestrial environments by plants</p><p>is one of the most significant events in the history of life. It remains</p><p>largely unknown why it is a lineage of charophytes that colonized</p><p>land (Box 1). The two tiers of innate immunity might provide the</p><p>genetic toolkits for early plants to fight against and co-opt microbes</p><p>in terrestrial environments (Gao et al., 2018). Indeed, both RLK</p><p>and NLR proteins underwent dramatic expansion during the</p><p>colonization of land by plants (Lehti-Shiu et al., 2009; Bowman</p><p>et al., 2017; Gao et al., 2018).</p><p>Besides the relatively young origin of the two tiers of innate</p><p>immunity, SA signaling might have originated during the emer-</p><p>gence of land plants (Wang et al., 2015). Given that many</p><p>chlorophytes, rhodophytes and glaucophytes engage in antagonis-</p><p>tic associations with pathogens, one question immediately arises:</p><p>How do these species fight against pathogens? RNAi does appear to</p><p>have an earlier origin than plants, possibly during the emergence of</p><p>eukaryotes, and might play some role in defense against pathogens</p><p>in these algal species. However, RNAi was lost multiple times</p><p>� 2018 The Author</p><p>New Phytologist� 2018 New Phytologist Trust</p><p>New Phytologist (2019) 222: 70–83</p><p>www.newphytologist.com</p><p>New</p><p>Phytologist Tansley review Review 79</p><p>14698137, 2019, 1, D</p><p>ow</p><p>nloaded from</p><p>https://nph.onlinelibrary.w</p><p>iley.com</p><p>/doi/10.1111/nph.15596 by M</p><p>ozam</p><p>bique H</p><p>inari N</p><p>PL</p><p>, W</p><p>iley O</p><p>nline L</p><p>ibrary on [31/08/2024]. See the T</p><p>erm</p><p>s and C</p><p>onditions (https://onlinelibrary.w</p><p>iley.com</p><p>/term</p><p>s-and-conditions) on W</p><p>iley O</p><p>nline L</p><p>ibrary for rules of use; O</p><p>A</p><p>articles are governed by the applicable C</p><p>reative C</p><p>om</p><p>m</p><p>ons L</p><p>icense</p><p>during the evolution of plants (and other eukaryotes) (Shabalina&</p><p>Koonin, 2008). Moreover, NLRs appear to be only sporadically</p><p>distributed in chlorophytes (Shao et al., 2018). It is possible that</p><p>plants employ other immune strategies. Proteins with scavenger</p><p>receptor cysteine-rich and C-type lectin domains, both of which</p><p>function in ligand binding and the innate immunity of animals, are</p><p>present in the chlorophyte C. reinhardtii (Wheeler et al., 2008).</p><p>Alternatively, some algae might not have to evolve or maintain</p><p>immunity, if pathogens only constitute a negligible risk to the algae,</p><p>the so called rare-enemy effect (Dawkins, 1982). After all,</p><p>maintaining immunity is somewhat costly (Stahl et al., 1999; Tian</p><p>et al., 2003; Karasov et al., 2014b). Further work to explore the</p><p>spectrum of pathogens and other possible immune strategies in</p><p>algae and nonflowering land plants might help us fully understand</p><p>the origin and evolution of the plant immune system.</p><p>Acknowledgements</p><p>We apologize to colleagues whose work were not cited due to space</p><p>limitations. 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