Abstract
Xylem is a plant vascular tissue that transports water and dissolved minerals from the roots to the rest of the plant. It consists of specialized water-conducting tracheary elements, supporting fibre cells and storage parenchyma cells. Certain plant pathogenic fungi, oomycetes and bacteria have evolved strategies to invade xylem vessels and cause highly destructive vascular wilt diseases that affect the crop production and forest ecosystems worldwide. In this chapter, we consider the molecular mechanisms of root-specific defence responses against vascular wilt pathogens, with an emphasis on the most important and well-studied fungal (Verticillium spp. and Fusarium oxysporum) and bacterial (Xanthomonas spp. and Ralstonia solanacearum) pathogens. In particular, we present the current understanding of plant immune responses, from invasion perception to signal transduction and termination. Furthermore, we address the role of specific transcription factors involved in plant immunity and their regulatory network. We also highlight the crucial roles of phytohormones as signalling molecules in local and systemic defence responses. Finally, we summarize the current knowledge of plant defence responses to xylem-invading pathogens to devise new strategies and methods for controlling these destructive plant pathogens.
Keywords
- Vascular wilt pathogens
- effectors
- plant innate immunity
- signal transduction
- biotic stress
1. Introduction
The disease triangle concept, introduced in the 1960s by George McNew to predict plant disease outcomes, shows the complex interactions among the environment, the host and the infectious (or abiotic) agent [1]. Plants, continuously challenged by numerous abiotic stresses, potential pests and pathogens, have evolved efficient strategies to perceive and respond to such threats. Plants lack specialized immune cells and their survival relies upon a highly sophisticated innate immune system, in which each plant cell responds autonomously [2–5]. The first line of defence is a basal resistance response called pattern-triggered immunity (PTI). It is induced by recognition of exogenous microbe or pathogen-associated molecular patterns (MAMPs or PAMPs) or endogenous molecules released on pathogen perception or pathogen-induced cell damage (damage-associated molecular patterns, DAMPs) via pattern-recognition receptors (PRRs) in the plasma membrane [4]. Successful pathogens overcome PTI by secreting effectors, hydrolytic enzymes or toxins, which suppress or interfere with host defence molecules [6]. In an evolutionary arms race, plants have evolved a robust defence response network termed effector-triggered immunity (ETI) to intercept pathogen effectors through intracellular receptors, such as nucleotide-binding site/leucine-rich repeat (NLR) proteins [5,7,8]. An intricate network of signalling pathways transduces these incoming signals into a diverse array of immune responses activating reactive oxygen species (ROS) generation, MAP kinases, Ca2+ signalling, the production of phytohormones and extensive transcriptional reprogramming [9].
In the past, comprehensive research has been dedicated to understanding plant physiological and molecular responses to individual abiotic and biotic stresses under controlled laboratory conditions. Recent studies of plant responses to concurrent abiotic and biotic stress conditions [10–16] have demonstrated that plants perceive and respond to combined stresses in a specific and unique manner. Moreover, the underlying signalling pathways are carefully modulated [14,17,18] and coordinated to ensure that plant growth and fitness are not significantly retarded [19].
Vascular wilt pathogens are soil-borne bacteria, fungi and oomycetes that employ various infection strategies to invade plant roots at different infection sites [20]. They subsequently advance inter- or intracellularly through the root cortex and enter the xylem vessels, where they proliferate and spread passively with xylem sap to aerial plant parts [21]. The characteristic wilt symptoms develop as a consequence of obstructed transportation of water and minerals, either due to the physical blockage of vessels by the pathogen or indirectly due to the activation of plant physical defence responses (e.g. formation of tyloses, accumulation of pectin-rich gels and gums) that confine the further spread of the pathogen [22]. In addition to wilting, other disease symptoms include vein clearing, leaf epinasty, chlorosis, vascular browning, stunting, necrosis and eventually plant death [21–24].
Primarily due to the specific lifestyle of vascular wilt pathogens, relatively little is known about their interactions with host plants and root-specific defence responses on molecular and biochemical levels compared to foliar pathogens. This chapter, therefore, summarizes the currently available molecular, cellular and systems biology data gathered from studies of signalling networks in model plants and crops challenged by bacterial or fungal pathogens and applies this general knowledge to advance understanding of vascular wilt pathogenesis and implement all these findings into the design of new strategies for the protection of crops and forest ecosystems.
2. Plant immune signalling initiation
Several factors contribute to the complex regulatory mechanisms in the initiation of plant immune signalling: (i) as sessile organisms, plants need to respond promptly to danger signals, (ii) each plant cell reacts autonomously to different stimuli, but the response needs to be integrated at a higher organizational level to ensure the plant’s survival and (iii) immune reactions are energy- and resource-demanding processes requiring the proper timing and amplitude of response [4]. Typically, immune responses occur on recognition of conserved microbe-, pathogen- or damage-associated molecular patterns or after perception of effector molecules that are species-, race-, or strain-specific and contribute to pathogen virulence [25]. However, not all microbial elicitors conform to the common distinction between PAMPs and effectors, and so Thomma et al. [26] proposed that plant immunity should be considered as a continuum, instead of a two-branched system composed of PAMP-triggered immunity (PTI) and effector-triggered immunity (ETI). An alternative perspective of plant innate immunity as a system that evolves to detect invasion has recently been extended into a so-called invasion model [27]. In this model, invasion patterns (IPs), externally encoded or modified-self ligands that signify invasion, are perceived by plant invasion pattern receptors (IPRs) and induce IP-triggered responses that do not result in immunity by default.
2.1. Plant PRRs convey danger signals to the intracellular immune signalling pathways
Recently emerging structural biology data on plant–pathogen interactions, [28] together with data obtained primarily from genetic and biochemical studies on the leaves of model plants and crops, have revealed that fine-tuning and coordination of immune responses are achieved within large protein complexes at the plasma membrane, where plant PRRs reside [4]. Plant PRRs are either receptor-like kinases (RLKs) or receptor-like proteins (RLPs) [4,6,25,29]. RLKs are modular proteins comprised of an extracellular domain involved in recognition of MAMPs/DAMPs, a single-pass transmembrane domain and a cytosolic serine/threonine kinase domain that transmits a signal to downstream signalling components. RLPs have a similar architecture, but their short cytoplasmic tail lacks kinase activity. RLPs, therefore, probably form heteromeric complexes with RLKs or other cytosolic kinases to relay downstream signalling. Extracellular domains of PRRs contain various motifs involved in recognition and binding of ligands. Leucine-rich repeat (LRR) motifs are widespread and serve as a scaffold for protein- or peptide–protein interactions [30]. Well-characterized examples of LRR–RLKs are
2.1.1. Perception of chitin
The chitin-responsive PRR system has been thoroughly investigated in both dicots and monocots. The perception of chitin in monocot plants is best described in rice (
The model dicot plant
2.1.2. Perception of flagellin
Extensive research of the model plant
2.1.3. Perception of peptidoglycan
Peptidoglycan (PGN), a polymer of N-acetylglucosamine and N-acetylmuramic acid branched with a short peptide, is an essential component of a bacterial cell wall and is another well-studied MAMP. In
2.1.4. Perception of DAMPs
Some PRRs respond to damage-associated molecular patterns (DAMPs), endogenous molecules such as cell wall fragments or peptides released on pathogen attack or various abiotic stresses [25,56]. Partial degradation of pectic polysaccharide homogalacturonan (HGA) by pathogen or plant polygalacturonases produces oligogalacturonides (OGs), oligomers of α-1,4–linked galacturonic acid [57,58]. In
The best studied peptides acting as DAMPs belong to the plant elicitor peptides (Peps) family. They are processed from precursor PROPEPs [61,62]. AtPep1, a 23 amino acid peptide released from the C-terminal of PROPEP1, was the first peptide elicitor isolated from
2.2. Intracellular immune receptors NLRs detect pathogen effectors
In addition to PRRs, plants have evolved a second class of immune receptors that intercept effectors in different parts of the cell [8]. These intracellular receptors, so called NLRs, are characterized as multi-domain proteins that have a conserved central nucleotide-binding (NB) domain and variable C-terminal leucine-rich repeats (LRR) domain [28]. In terms of their distinct N-terminal domains, NLRs are broadly divided into two groups: TNLs that harbour a Toll–interleukin 1 receptor (TIR) domain and CNLs that contain a coiled-coil (CC) domain [69–71]. NLRs belong to signal transduction ATPases with numerous domains (STAND) that operate as molecular switches cycling between an inactive closed ADP-bound state and active open state with bound GTP [72–74]. In the resting state, N-terminal TIR or CC and C-terminal LRR domains sterically inhibit the NB domain from ADP–ATP exchange. On pathogen recognition, a series of conformational changes occur that expose the NB domain, promote ADP–ATP exchange and initiate signal transduction [8]. Effector recognition by NLRs often, but not always, leads to a form of programmed cell death termed as a hypersensitive response [75]. NLRs are, therefore, under precise control by accessory proteins. NLRs interact with conserved Hsp90-Sgt1-RAR1 protein complexes for proper folding, accumulation and regulation [76,77]. Moreover, Sgt1 interacts with the suppressor of
Various strategies of effector recognition by NLRs exist and are represented in different models. In the gene-for-gene model, originally described by Flor in 1971, NLRs can recognize effectors directly (e.g.
Activated NLRs trigger a variety of immune responses, from the generation of ROS, elevation of intracellular Ca2+, activation of MAPK cascades, transcriptional reprogramming to production of phytohormones [8]. Although effector-triggered responses are qualitatively similar to immune responses elicited by MAMPs/DAMPs, there are quantitative differences in the strength and duration of pathways, which result in different resistance responses and signalling networks [17].
2.3. Signal transduction cascades
Perception of MAMPs/DAMPs by their cognate receptors triggers an array of immune responses, comprising changes in intracellular calcium levels [Ca2+]i, membrane potential depolarization, extracellular alkalinization, production of ROS, NO and phosphatidic acid, activation of kinases (mitogen-activated protein kinases (MAPKs) or Ca2+-dependent protein kinases (CDPKs)), transcriptional reprogramming and changes in plant hormone concentrations (e.g. ethylene, salicylic and jasmonic acid) [88,89].
2.3.1. Calcium and ROS signalling interconnection
Ca2+ is a ubiquitous second messenger released in response to various stresses and developmental processes. In
Rapid production of reactive oxygen species (ROS) in response to MAMPs/DAMPs depends primarily on respiratory burst oxidase homologues (RBOHs) [92,93]. These NADPH oxidases are integral membrane proteins that generate superoxide anions (O2−), which are rapidly converted into hydrogen peroxide (H2O2). RBOHs have cytosolic FAD- and NADPH-binding domains in the C-terminal region, six membrane-spanning domains and a cytosolic N-terminal extension that harbours two EF-hand motifs and multiple phosphorylation sites [94]. Recent studies in
2.3.2. MAPK signalling
Plant mitogen-activated protein kinase (MAPK) cascades generally comprise MAPKK kinases (or MEKKs), which receive signals from receptors/sensors and phosphorylate downstream MAPK kinases (or MKKs) and which subsequently activate MAPKs (or MPKs) that control the activities and synthesis of a plethora of transcription factors (TFs), enzymes, hormones, peptides and antimicrobial chemicals [101,102]. In
2.4. Transcriptional reprogramming converges with complex phytohormone signalling networks
Transcription factors (TFs) involved in plant immunity reside in transcriptional complexes and, together with co-regulatory proteins, directly or indirectly recruit RNA polymerase II to the target promoters or release it from them [116]. TFs vital for plant immunity comprise members of the AP2/ERF, bHLH, bZIP, MYB, NAC and WRKY TF families and perform diverse roles [9]. For instance, certain members of apetala2/ethylene-response element binding factor (AP2/ERF) participate in the regulation of genes related to the jasmonic acid (JA) and ethylene hormone signalling pathways [117].
TF expression and activities are regulated in multiple ways. Certain nucleotide-binding site/leucine-rich repeat (NLR) proteins directly regulate transcription by physically interacting with TFs [120–123]. Several TFs are controlled by phosphorylation as downstream targets of activated MAPK cascades [109,124–127]. Another mechanism of TFs activation is carried out by Ca2+sensors such as CaMs and CDPKs [128–133]. Additional factors (e.g. components of mediator complex [134,135], chromatin modifications [136–138]) and levels of regulation (e.g. ubiquitination [139], sumoylation [140], alternative mRNA splicing [141]) also contribute to the complexity of transcriptional networks and fine-tuning of immune responses.
Coordination of diverse stress responses and growth is resolved within complex phytohormone signalling networks, in which salicylic acid (SA), jasmonic acid (JA) and ethylene (ET) perform central roles, while other hormones merely modulate their responses [142]. SA is synthesized in chloroplasts from chorismate by isochorismate synthase [143] and exported to the cytosol [144]. In response to pathogens and various abiotic stresses, SA mediates expression of pathogenesis-related (PR) genes and the synthesis of antimicrobial compounds to provide basal defence and systemic acquired resistance (SAR) [145]. SA activates these defence responses through transcription cofactor nonexpresser of PR genes 1 (NPR1) [146] and transcription factors TGA2, TGA5 and TGA6 [119]. In the absence of SA, NPR1 is sequestered in the cytosol and forms oligomeric complexes stabilized by intermolecular disulphide bonds [147]. In response to activation of SA pathway, thioredoxins reduce these disulphide bonds, causing the release of NPR1 in monomeric form, which can translocate to the nucleus via a nuclear translocation signal (NLS) [148]. In addition, NPR1 protein levels oscillate through CUL3NPR3- and CUL3NPR4-mediated degradation in the nucleus, which is required for fine-tuning of immune responses [147,149,150].
Jasmonates (JAs) are plant hormones with essential roles in plant defence and development [118]. JAs are derived from
Ethylene (ET) is a gaseous hormone that often works synergistically with JA [156]. Important steps in ET biosynthesis are the conversion of
Plant hormonal crosstalk is extensive and occurs in several combinations [163]. The molecular mechanism underlying SA-mediated reprogramming of the JA transcriptional network points to immune signalling antagonism and the involvement of transcriptional regulators NPR1, TGA, WRKY and ORA59 as signal integrators [164]. Phytohormones JA and ET synergistically regulate plant defence responses to necrotrophic fungi via JA-induced EIN3 and EIL1 activation and ET-induced EIN3 and EIL1 stabilization. In addition, antagonistic effects observed in JA and ET signalling are mediated by the interaction of JA-activated MYC2 TF and ET-stabilized TF EIN3 [165].
2.5. Inactivation of immune signalling pathways
Various negative regulation mechanisms ensure immune signalling activation is switched off when there is no danger. In the absence of ligand, several phosphatases interact with PRRs and their associated kinases to keep immune complexes inactive through dephosphorylation. For instance, Ser/Thr phosphatase type 2A (PP2A) constitutively associates with BRI1-associated kinase1 (BAK1) and negatively controls BAK1 activation in PRR immune receptor complexes [166]. Negative regulation exerted by downstream phosphatases is illustrated by
Ubiquitination and proteasomal degradation are other mechanisms by which plant immune responses are attenuated. For example, two U-box E3 ubiquitin ligases, PUB12 and PUB13, are recruited to flagellin-induced FLS2/BAK1 receptor complex and phosphorylated by BAK1 to polyubiquitinate FLS2 and promote its degradation [168]. Downregulation of immune signalling can also be achieved by ligand-induced endocytosis and degradation [169]. This has been reported in localization studies of flg22-induced FLS2 receptors in
3. Plant defence responses to xylem-invading pathogens
3.1. General perception of MAMPs in roots
Despite the fact that roots are subjected to a rich microbial community, the perception of MAMPs and immune responses in roots are poorly understood. Millet et al. [172] studied immune responses in
3.2. Perception of vascular wilt pathogens
At early stages of infection, vascular wilt pathogens are faced with preformed physical and chemical root defences and MAMP-induced immune responses that hinder their invasion [20]. Once they breach the rigid secondary xylem walls and enter the xylem vessels, vascular wilt pathogens are presumably recognized by specific extracellular receptors in the parenchyma cells surrounding the xylem vessels [21].
3.2.1. Perception of Verticillium spp.
In tomato, extracellular LRR RLP Ve1 [24,175,176] plays a role in xylem defence and provides resistance against race 1 strains of
Ve1 forms heterodimers with a tomato orthologue of the
3.2.2. Perception of Fusarium oxysporum f. sp. lycopersici
Three I (immunity) genes have been identified in tomato [184] in a resistance response to
3.2.3. Perception of Xanthomonas oryzae pv. oryzae
The rice LRR RLK Xa21 that provides resistance to
3.2.4. Perception of Ralstonia solanacearum
A pair of
3.3. Induced defence responses to vascular wilt pathogens
Recognition of vascular wilt pathogens by plant immune receptor complexes activates defence responses in the xylem vessels. Physical defence responses that confine pathogens from further spread comprise the formation of tyloses, accumulation of pectin-rich gels and gums, vascular coating and callose and secondary cell wall deposition [20,21]. An interesting adaptation to vascular wilt infection is vein clearing, a tissue-specific developmental programme leading to the formation of new xylem elements [207]. Furthermore, significant metabolic changes have been reported in response to xylem infection and involve the induction of pathogenesis-related (PR) proteins, peroxidases, proteases as well as the production of antimicrobial secondary metabolites such as phytoalexins, sulphur-containing compounds and phenolic compounds [20,21].
Studies of defence signalling in response to root pathogens have so far mainly focused on the leaves and have provided evidence that defence mechanisms involve similar signalling pathways (Ca2+-signalling, induction of ROS and MAPK cascades, modulation of phytohormone signalling) [20]. Moreover, plant microarray and RNASeq studies have revealed that the interaction between vascular wilt pathogens and host plants involves transcriptional reprogramming of hundreds of genes [208–211]. Interestingly, in an incompatible interaction, only modest changes in gene and protein expression have been reported [210,212–214] and most of the differentially expressed genes have been repressed in roots rather than in leaves [211]. Moreover, genes implicated in photorespiration, hypoxia, glycoxylate metabolism and auxin signalling show inverse regulation on infection with the foliar pathogen
Genome-wide analyses on transcriptional and proteomic levels, together with functional characterization of individual genes, have revealed a convergence of signalling pathways in response to individual pathogens, in mostly controlled conditions. In the field, plants are simultaneously challenged by multiple stress factors, both biotic and abiotic. Even though signalling components of plant regulatory networks are partly shared in both and point to general stress response mechanisms, there is evidence of specific responses to combined stresses that are controlled by different signalling pathways and such studies may provide additional candidates for crop protection breeding [14–16,18].
References
- 1.
Scholthof K-BG. The disease triangle: pathogens, the environment and society. Nat Rev Microbiol. Nature Publishing Group; 2006 Dec 27;5(2):152–6. - 2.
Jones JDG, Dangl JL. The plant immune system. Nature. 2006 Nov 16;444(7117):323–9. - 3.
Dodds PN, Rathjen JP. Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev Genet. 2010 Aug;11(8):539–48. - 4.
Macho AP, Zipfel C. Plant PRRs and the activation of innate immune signaling. Mol Cell. 2014 Apr 24;54(2):263–72. - 5.
Cesari S, Bernoux M, Moncuquet P, Kroj T, Dodds PN. A novel conserved mechanism for plant NLR protein pairs: the “integrated decoy” hypothesis. Front Plant Sci. 2014 Jan;5:606. - 6.
Trdá L, Boutrot F, Claverie J, Brulé D, Dorey S, Poinssot B. Perception of pathogenic or beneficial bacteria and their evasion of host immunity: pattern recognition receptors in the frontline. Front Plant Sci. Frontiers; 2015 Apr 8;6:219. - 7.
Bonardi V, Cherkis K, Nishimura MT, Dangl JL. A new eye on NLR proteins: focused on clarity or diffused by complexity? Curr Opin Immunol. 2012 Feb;24(1):41–50. - 8.
Cui H, Tsuda K, Parker JE. Effector-triggered immunity: from pathogen perception to robust defense. Annu Rev Plant Biol. 2015 Jan;66:487–511. - 9.
Tsuda K, Somssich IE. Transcriptional networks in plant immunity. New Phytol. 2015 Jan 26;206(3):932–47. - 10.
Atkinson NJ, Lilley CJ, Urwin PE. Identification of genes involved in the response of Arabidopsis to simultaneous biotic and abiotic stresses. Plant Physiol. 2013 Aug 1;162(4):2028–41. - 11.
Rasmussen S, Barah P, Suarez-Rodriguez MC, Bressendorff S, Friis P, Costantino P, et al. Transcriptome responses to combinations of stresses in Arabidopsis . Plant Physiol. 2013 Apr;161(4):1783–94. - 12.
Bostock RM, Pye MF, Roubtsova T V. Predisposition in plant disease: exploiting the nexus in abiotic and biotic stress perception and response. Annu Rev Phytopathol. 2014 Jan;52:517–49. - 13.
Prasch CM, Sonnewald U. Simultaneous application of heat, drought, and virus to Arabidopsis plants reveals significant shifts in signaling networks. Plant Physiol. 2013 Aug;162(4):1849–66. - 14.
Atkinson NJ, Jain R, Urwin PE. The Response of Plants to Simultaneous Biotic and Abiotic Stress. In: Mahalingam R, editor. Combined Stresses in Plants SE - 9. Springer International Publishing; 2015. pp. 181–201. - 15.
Suzuki N, Rivero RM, Shulaev V, Blumwald E, Mittler R. Abiotic and biotic stress combinations. New Phytol. 2014 Jul 11;203(1):32–43. - 16.
Kissoudis C, van de Wiel C, Visser RGF, van der Linden G. Enhancing crop resilience to combined abiotic and biotic stress through the dissection of physiological and molecular crosstalk. Front Plant Sci. 2014 Jan;5:207. - 17.
Tsuda K, Katagiri F. Comparing signaling mechanisms engaged in pattern-triggered and effector-triggered immunity. Curr Opin Plant Biol. 2010 Aug;13(4):459–65. - 18.
Atkinson NJ, Urwin PE. The interaction of plant biotic and abiotic stresses: from genes to the field. J Exp Bot. 2012 Jun 30;63(10):3523–43. - 19.
Denancé N, Sánchez-Vallet A, Goffner D, Molina A. Disease resistance or growth: the role of plant hormones in balancing immune responses and fitness costs. Front Plant Sci. Frontiers; 2013 Jan 24;4:155. - 20.
De Coninck B, Timmermans P, Vos C, Cammue BPA, Kazan K. What lies beneath: belowground defense strategies in plants. Trends Plant Sci. 2015 Oct;20(2):91–101. - 21.
Yadeta KA, J Thomma BPH. The xylem as battleground for plant hosts and vascular wilt pathogens. Front Plant Sci. 2013 Jan;4:97. - 22.
Doohan F. Fungal Pathogens of Plants. Fungi. John Wiley & Sons, Ltd; 2011. pp. 313–344. - 23.
Pietro A Di, Madrid MP, Caracuel Z, Delgado-Jarana J, Roncero MIG. Fusarium oxysporum : exploring the molecular arsenal of a vascular wilt fungus. Mol Plant Pathol. 2003 Sep 1;4(5):315–25. - 24.
Fradin EF, Thomma BPHJ. Physiology and molecular aspects of Verticillium wilt diseases caused byV. dahliae andV. albo-atrum . Mol Plant Pathol. Blackwell Publishing Ltd; 2006;7(2):71–86. - 25.
Boller T, Felix G. A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol. 2009 Jan;60:379–406. - 26.
Thomma BPHJ, Nürnberger T, Joosten MHAJ. Of PAMPs and effectors: the blurred PTI-ETI dichotomy. Plant Cell. 2011 Jan;23(1):4–15. - 27.
Cook DE, Mesarich CH, Thomma BPHJ. Understanding Plant Immunity as a Surveillance System to Detect Invasion. Annu Rev Phytopathol. 2015 Jun 5;53:541–63. - 28.
Wirthmueller L, Maqbool A, Banfield MJ. On the front line: structural insights into plant-pathogen interactions. Nat Rev Microbiol. Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved.; 2013 Nov;11(11):761–76. - 29.
Holton N, Nekrasov V, Ronald PC, Zipfel C. The phylogenetically-related pattern recognition receptors EFR and XA21 recruit similar immune signaling components in monocots and dicots. PLoS Pathog. Public Library of Science; 2015 Jan 21;11(1):e1004602. - 30.
Matsushima N, Miyashita H. Leucine-Rich Repeat (LRR) Domains Containing Intervening Motifs in Plants. Biomolecules. 2012 Jan;2(2):288–311. - 31.
Gómez-Gómez L, Boller T. FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis . Mol Cell. 2000 Jun;5(6):1003–11. - 32.
Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones JDG, Boller T, et al. Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium -mediated transformation. Cell. 2006 May 19;125(4):749–60. - 33.
Miya A, Albert P, Shinya T, Desaki Y, Ichimura K, Shirasu K, et al. CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis . Proc Natl Acad Sci U S A. 2007 Dec 4;104(49):19613–8. - 34.
Petutschnig EK, Jones AME, Serazetdinova L, Lipka U, Lipka V. The lysin motif receptor-like kinase (LysM-RLK) CERK1 is a major chitin-binding protein in Arabidopsis thaliana and subject to chitin-induced phosphorylation. J Biol Chem. 2010 Sep 10;285(37):28902–11. - 35.
Willmann R, Lajunen HM, Erbs G, Newman M-A, Kolb D, Tsuda K, et al. Arabidopsis lysin-motif proteins LYM1 LYM3 CERK1 mediate bacterial peptidoglycan sensing and immunity to bacterial infection. Proc Natl Acad Sci U S A. 2011 Dec 6;108(49):19824–9. - 36.
Kaku H, Nishizawa Y, Ishii-Minami N, Akimoto-Tomiyama C, Dohmae N, Takio K, et al. Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc Natl Acad Sci U S A. 2006 Jul 18;103(29):11086–91. - 37.
Shimizu T, Nakano T, Takamizawa D, Desaki Y, Ishii-Minami N, Nishizawa Y, et al. Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant J. 2010 Oct;64(2):204–14. - 38.
Hayafune M, Berisio R, Marchetti R, Silipo A, Kayama M, Desaki Y, et al. Chitin-induced activation of immune signaling by the rice receptor CEBiP relies on a unique sandwich-type dimerization. Proc Natl Acad Sci U S A. 2014 Jan 21;111(3):E404–13. - 39.
Akamatsu A, Wong HL, Fujiwara M, Okuda J, Nishide K, Uno K, et al. An OsCEBiP/OsCERK1-OsRacGEF1-OsRac1 module is an essential early component of chitin-induced rice immunity. Cell Host Microbe. 2013 Apr 17;13(4):465–76. - 40.
Kosami K, Ohki I, Nagano M, Furuita K, Sugiki T, Kawano Y, et al. The crystal structure of the plant small GTPase OsRac1 reveals its mode of binding to NADPH oxidase. J Biol Chem. 2014 Oct 10;289(41):28569–78. - 41.
Liu T, Liu Z, Song C, Hu Y, Han Z, She J, et al. Chitin-induced dimerization activates a plant immune receptor. Science. 2012 Jun 1;336(6085):1160–4. - 42.
Cao Y, Liang Y, Tanaka K, Nguyen CT, Jedrzejczak RP, Joachimiak A, et al. The kinase LYK5 is a major chitin receptor in Arabidopsis and forms a chitin-induced complex with related kinase CERK1. Elife. 2014 Jan;3:e03766. - 43.
Chinchilla D, Bauer Z, Regenass M, Boller T, Felix G. The Arabidopsis receptor kinase FLS2 binds flg22 and determines the specificity of flagellin perception. Plant Cell. 2006 Feb;18(2):465–76. - 44.
Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nürnberger T, Jones JDG, et al. A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature. 2007 Jul 26;448(7152):497–500. - 45.
Roux M, Schwessinger B, Albrecht C, Chinchilla D, Jones A, Holton N, et al. The Arabidopsis leucine-rich repeat receptor-like kinases BAK1/SERK3 and BKK1/SERK4 are required for innate immunity to hemibiotrophic and biotrophic pathogens. Plant Cell. 2011 Jun;23(6):2440–55. - 46.
Sun Y, Li L, Macho AP, Han Z, Hu Z, Zipfel C, et al. Structural basis for flg22-induced activation of the Arabidopsis FLS2-BAK1 immune complex. Science. 2013 Nov 1;342(6158):624–8. - 47.
Belkhadir Y, Yang L, Hetzel J, Dangl JL, Chory J. The growth-defense pivot: crisis management in plants mediated by LRR-RK surface receptors. Trends Biochem Sci. Elsevier; 2014 Oct 10;39(10):447–56. - 48.
Heese A, Hann DR, Gimenez-Ibanez S, Jones AME, He K, Li J, et al. The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc Natl Acad Sci U S A. 2007 Jul 17;104(29):12217–22. - 49.
Li J, Wen J, Lease KA, Doke JT, Tax FE, Walker JC. BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell. 2002 Jul 26;110(2):213–22. - 50.
Lu D, Wu S, Gao X, Zhang Y, Shan L, He P. A receptor-like cytoplasmic kinase, BIK1, associates with a flagellin receptor complex to initiate plant innate immunity. Proc Natl Acad Sci U S A. 2010 Jan 5;107(1):496–501. - 51.
Lin W, Li B, Lu D, Chen S, Zhu N, He P, et al. Tyrosine phosphorylation of protein kinase complex BAK1/BIK1 mediates Arabidopsis innate immunity. Proc Natl Acad Sci U S A. 2014 Mar 4;111(9):3632–7. - 52.
Ranf S, Eschen-Lippold L, Fröhlich K, Westphal L, Scheel D, Lee J. Microbe-associated molecular pattern-induced calcium signaling requires the receptor-like cytoplasmic kinases, PBL1 and BIK1. BMC Plant Biol. 2014 Jan;14:374. - 53.
Li L, Li M, Yu L, Zhou Z, Liang X, Liu Z, et al. The FLS2-associated kinase BIK1 directly phosphorylates the NADPH oxidase RbohD to control plant immunity. Cell Host Microbe. 2014 Mar 12;15(3):329–38. - 54.
Ao Y, Li Z, Feng D, Xiong F, Liu J, Li J-F, et al. OsCERK1 and OsRLCK176 play important roles in peptidoglycan and chitin signaling in rice innate immunity. Plant J. 2014 Dec;80(6):1072–84. - 55.
Liu B, Li J-F, Ao Y, Qu J, Li Z, Su J, et al. Lysin motif-containing proteins LYP4 and LYP6 play dual roles in peptidoglycan and chitin perception in rice innate immunity. Plant Cell. 2012 Aug;24(8):3406–19. - 56.
Albert M. Peptides as triggers of plant defence. J Exp Bot. 2013 Dec 1;64(17):5269–79. - 57.
Ferrari S, Savatin D V, Sicilia F, Gramegna G, Cervone F, Lorenzo G De. Oligogalacturonides: plant damage-associated molecular patterns and regulators of growth and development. Front Plant Sci. 2013 Jan;4:49. - 58.
Benedetti M, Pontiggia D, Raggi S, Cheng Z, Scaloni F, Ferrari S, et al. Plant immunity triggered by engineered in vivo release of oligogalacturonides, damage-associated molecular patterns. Proc Natl Acad Sci U S A. 2015 Apr 28;112(17):5533–8. - 59.
Brutus A, Sicilia F, Macone A, Cervone F, De Lorenzo G. A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides. Proc Natl Acad Sci U S A. 2010 May 18;107(20):9452–7. - 60.
Galletti R, Ferrari S, De Lorenzo G. Arabidopsis MPK3 and MPK6 play different roles in basal and oligogalacturonide- or flagellin-induced resistance againstBotrytis cinerea . Plant Physiol. 2011 Oct 1;157(2):804–14. - 61.
Huffaker A, Pearce G, Ryan CA. An endogenous peptide signal in Arabidopsis activates components of the innate immune response. Proc Natl Acad Sci U S A. 2006 Jun 27;103(26):10098–103. - 62.
Huffaker A, Ryan CA. Endogenous peptide defense signals in Arabidopsis differentially amplify signaling for the innate immune response. Proc Natl Acad Sci U S A. 2007 Jun 19;104(25):10732–6. - 63.
Yamaguchi Y, Huffaker A. Endogenous peptide elicitors in higher plants. Curr Opin Plant Biol. 2011 Aug;14(4):351–7. - 64.
Yamaguchi Y, Pearce G, Ryan CA. The cell surface leucine-rich repeat receptor for AtPep1, an endogenous peptide elicitor in Arabidopsis , is functional in transgenic tobacco cells. Proc Natl Acad Sci U S A. 2006 Jun 27;103(26):10104–9. - 65.
Yamaguchi Y, Huffaker A, Bryan AC, Tax FE, Ryan CA. PEPR2 is a second receptor for the Pep1 and Pep2 peptides and contributes to defense responses in Arabidopsis . Plant Cell. 2010 Feb;22(2):508–22. - 66.
Postel S, Küfner I, Beuter C, Mazzotta S, Schwedt A, Borlotti A, et al. The multifunctional leucine-rich repeat receptor kinase BAK1 is implicated in Arabidopsis development and immunity. Eur J Cell Biol. Jan;89(2-3):169–74. - 67.
Qi Z, Verma R, Gehring C, Yamaguchi Y, Zhao Y, Ryan CA, et al. Ca2+ signaling by plant Arabidopsis thaliana Pep peptides depends on AtPepR1, a receptor with guanylyl cyclase activity, and cGMP-activated Ca2+ channels. Proc Natl Acad Sci U S A. 2010 Dec 7;107(49):21193–8. - 68.
Ma Y, Walker RK, Zhao Y, Berkowitz GA. Linking ligand perception by PEPR pattern recognition receptors to cytosolic Ca2+ elevation and downstream immune signaling in plants. Proc Natl Acad Sci U S A. 2012 Nov 27;109(48):19852–7. - 69.
Collier SM, Moffett P. NB-LRRs work a “bait and switch” on pathogens. Trends Plant Sci. 2009 Oct;14(10):521–9. - 70.
Maekawa T, Kufer TA, Schulze-Lefert P. NLR functions in plant and animal immune systems: so far and yet so close. Nat Immunol. 2011 Sep;12(9):817–26. - 71.
Griebel T, Maekawa T, Parker JE. NOD-like receptor cooperativity in effector-triggered immunity. Trends Immunol. 2014 Nov;35(11):562–70. - 72.
Danot O, Marquenet E, Vidal-Ingigliardi D, Richet E. Wheel of Life, Wheel of Death: A Mechanistic Insight into Signaling by STAND Proteins. Structure. 2009 Mar 13;17(2):172–82. - 73.
Takken FLW, Tameling WIL. To nibble at plant resistance proteins. Science. 2009 May 8;324(5928):744–6. - 74.
Lukasik E, Takken FLW. STANDing strong, resistance proteins instigators of plant defence. Curr Opin Plant Biol. 2009 Aug;12(4):427–36. - 75.
Coll NS, Epple P, Dangl JL. Programmed cell death in the plant immune system. Cell Death Differ. Macmillan Publishers Limited; 2011 Aug;18(8):1247–56. - 76.
Elmore JM, Lin Z-JD, Coaker G. Plant NB-LRR signaling: upstreams and downstreams. Curr Opin Plant Biol. 2011 Aug;14(4):365–71. - 77.
Zhang M, Kadota Y, Prodromou C, Shirasu K, Pearl LH. Structural basis for assembly of Hsp90-Sgt1-CHORD protein complexes: implications for chaperoning of NLR innate immunity receptors. Mol Cell. 2010 Jul 30;39(2):269–81. - 78.
Li Y, Li S, Bi D, Cheng YT, Li X, Zhang Y. SRFR1 negatively regulates plant NB-LRR resistance protein accumulation to prevent autoimmunity. PLoS Pathog. 2010 Jan;6(9):e1001111. - 79.
Jia Y, McAdams SA, Bryan GT, Hershey HP, Valent B. Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO J. 2000 Aug 1;19(15):4004–14. - 80.
Tang X, Frederick R, Zhou J, Halterman D, Jia Y, Martin G. Initiation of Plant Disease Resistance by Physical Interaction of AvrPto and Pto Kinase. Science. 1996 Dec 20;274(5295):2060–3. - 81.
Van Der Biezen EA, Jones JDG. Plant disease-resistance proteins and the gene-for-gene concept. Trends Biochem Sci. 1998 Dec;23(12):454–6. - 82.
Van der Hoorn RAL, De Wit PJGM, Joosten MHAJ. Balancing selection favors guarding resistance proteins. Trends Plant Sci. 2002 Mar;7(2):67–71. - 83.
Marathe R, Dinesh-Kumar SP. Plant defense: one post, multiple guards?! Mol Cell. 2003 Mar;11(2):284–6. - 84.
Van der Hoorn RAL, Kamoun S. From Guard to Decoy: a new model for perception of plant pathogen effectors. Plant Cell. 2008 Aug;20(8):2009–17. - 85.
Ade J, DeYoung BJ, Golstein C, Innes RW. Indirect activation of a plant nucleotide binding site-leucine-rich repeat protein by a bacterial protease. Proc Natl Acad Sci U S A. 2007 Mar 13;104(7):2531–6. - 86.
Shao F, Golstein C, Ade J, Stoutemyer M, Dixon JE, Innes RW. Cleavage of Arabidopsis PBS1 by a bacterial type III effector. Science. 2003 Aug 29;301(5637):1230–3. - 87.
Zhang J, Li W, Xiang T, Liu Z, Laluk K, Ding X, et al. Receptor-like cytoplasmic kinases integrate signaling from multiple plant immune receptors and are targeted by a Pseudomonas syringae effector. Cell Host Microbe. 2010 Apr 22;7(4):290–301. - 88.
Seybold H, Trempel F, Ranf S, Scheel D, Romeis T, Lee J. Ca 2+ signalling in plant immune response: from pattern recognition receptors to Ca 2+ decoding mechanisms. New Phytol. 2014 Dec 24;204(4):782–90. - 89.
Wu S, Shan L, He P. Microbial signature-triggered plant defense responses and early signaling mechanisms. Plant Sci. 2014 Nov;228:118–26. - 90.
Ranf S, Eschen-Lippold L, Pecher P, Lee J, Scheel D. Interplay between calcium signalling and early signalling elements during defence responses to microbe- or damage-associated molecular patterns. Plant J. 2011 Oct;68(1):100–13. - 91.
Steinhorst L, Kudla J. Calcium and reactive oxygen species rule the waves of signaling. Plant Physiol. 2013 Oct 1;163(2):471–85. - 92.
Suzuki N, Miller G, Morales J, Shulaev V, Torres MA, Mittler R. Respiratory burst oxidases: the engines of ROS signaling. Curr Opin Plant Biol. 2011 Dec;14(6):691–9. - 93.
Baxter A, Mittler R, Suzuki N. ROS as key players in plant stress signalling. J Exp Bot. 2014 Mar;65(5):1229–40. - 94.
Glyan’ko AK, Ischenko AA. Structural and functional characteristics of plant NADPH oxidase: A review. Appl Biochem Microbiol. 2010 Sep 11;46(5):463–71. - 95.
Drerup MM, Schlücking K, Hashimoto K, Manishankar P, Steinhorst L, Kuchitsu K, et al. The Calcineurin B-like calcium sensors CBL1 and CBL9 together with their interacting protein kinase CIPK26 regulate the Arabidopsis NADPH oxidase RBOHF. Mol Plant. 2013 Mar;6(2):559–69. - 96.
Ogasawara Y, Kaya H, Hiraoka G, Yumoto F, Kimura S, Kadota Y, et al. Synergistic activation of the Arabidopsis NADPH oxidase AtrbohD by Ca2+ and phosphorylation. J Biol Chem. 2008 Apr 4;283(14):8885–92. - 97.
Kimura S, Kaya H, Kawarazaki T, Hiraoka G, Senzaki E, Michikawa M, et al. Protein phosphorylation is a prerequisite for the Ca2+-dependent activation of Arabidopsis NADPH oxidases and may function as a trigger for the positive feedback regulation of Ca2+ and reactive oxygen species. Biochim Biophys Acta. 2012 Feb;1823(2):398–405. - 98.
Dubiella U, Seybold H, Durian G, Komander E, Lassig R, Witte C-P, et al. Calcium-dependent protein kinase/NADPH oxidase activation circuit is required for rapid defense signal propagation. Proc Natl Acad Sci U S A. 2013 May 21;110(21):8744–9. - 99.
Miller G, Schlauch K, Tam R, Cortes D, Torres MA, Shulaev V, et al. The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci Signal. 2009 Jan 18;2(84):ra45. - 100.
Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, et al. ROS signaling: the new wave? Trends Plant Sci. 2011 Jun;16(6):300–9. - 101.
Tena G, Boudsocq M, Sheen J. Protein kinase signaling networks in plant innate immunity. Curr Opin Plant Biol. 2011 Oct;14(5):519–29. - 102.
Popescu SC, Popescu G V, Bachan S, Zhang Z, Gerstein M, Snyder M, et al. MAPK target networks in Arabidopsis thaliana revealed using functional protein microarrays. Genes Dev. 2009 Jan 1;23(1):80–92. - 103.
Asai T, Tena G, Plotnikova J, Willmann MR, Chiu W-L, Gomez-Gomez L, et al. MAP kinase signalling cascade in Arabidopsis innate immunity. Nature. 2002 Mar 28;415(6875):977–83. - 104.
Gao M, Liu J, Bi D, Zhang Z, Cheng F, Chen S, et al. MEKK1, MKK1/MKK2 and MPK4 function together in a mitogen-activated protein kinase cascade to regulate innate immunity in plants. Cell Res. 2008 Dec;18(12):1190–8. - 105.
Xu J, Xie J, Yan C, Zou X, Ren D, Zhang S. A chemical genetic approach demonstrates that MPK3/MPK6 activation and NADPH oxidase-mediated oxidative burst are two independent signaling events in plant immunity. Plant J. 2014 Jan;77(2):222–34. - 106.
Rodriguez MCS, Petersen M, Mundy J. Mitogen-activated protein kinase signaling in plants. Annu Rev Plant Biol. Annual Reviews; 2010 Jan 4;61:621–49. - 107.
Kong Q, Qu N, Gao M, Zhang Z, Ding X, Yang F, et al. The MEKK1-MKK1/MKK2-MPK4 kinase cascade negatively regulates immunity mediated by a mitogen-activated protein kinase kinase kinase in Arabidopsis . Plant Cell. 2012 May;24(5):2225–36. - 108.
Ren D, Liu Y, Yang K-Y, Han L, Mao G, Glazebrook J, et al. A fungal-responsive MAPK cascade regulates phytoalexin biosynthesis in Arabidopsis . Proc Natl Acad Sci U S A. 2008 Apr 8;105(14):5638–43. - 109.
Mao G, Meng X, Liu Y, Zheng Z, Chen Z, Zhang S. Phosphorylation of a WRKY transcription factor by two pathogen-responsive MAPKs drives phytoalexin biosynthesis in Arabidopsis . Plant Cell. 2011 Apr;23(4):1639–53. - 110.
Beckers GJM, Jaskiewicz M, Liu Y, Underwood WR, He SY, Zhang S, et al. Mitogen-activated protein kinases 3 and 6 are required for full priming of stress responses in Arabidopsis thaliana . Plant Cell. 2009 Mar;21(3):944–53. - 111.
Han L, Li G-J, Yang K-Y, Mao G, Wang R, Liu Y, et al. Mitogen-activated protein kinase 3 and 6 regulate Botrytis cinerea -induced ethylene production inArabidopsis . Plant J. 2010 Oct;64(1):114–27. - 112.
Ren D, Yang H, Zhang S. Cell death mediated by MAPK is associated with hydrogen peroxide production in Arabidopsis . J Biol Chem. 2002 Jan 4;277(1):559–65. - 113.
Zhao C, Nie H, Shen Q, Zhang S, Lukowitz W, Tang D. EDR1 physically interacts with MKK4/MKK5 and negatively regulates a MAP kinase cascade to modulate plant innate immunity. PLoS Genet. 2014 Jan;10(5):e1004389. - 114.
Frei dit Frey N, Garcia AV, Bigeard J, Zaag R, Bueso E, Garmier M, et al. Functional analysis of Arabidopsis immune-related MAPKs uncovers a role for MPK3 as negative regulator of inducible defences. Genome Biol. 2014 Jan;15(6):R87. - 115.
Lumbreras V, Vilela B, Irar S, Solé M, Capellades M, Valls M, et al. MAPK phosphatase MKP2 mediates disease responses in Arabidopsis and functionally interacts with MPK3 and MPK6. Plant J. 2010 Sep;63(6):1017–30. - 116.
Moore JW, Loake GJ, Spoel SH. Transcription dynamics in plant immunity. Plant Cell. 2011 Aug;23(8):2809–20. - 117.
Licausi F, Ohme-Takagi M, Perata P. APETALA2/Ethylene Responsive Factor (AP2/ERF) transcription factors: mediators of stress responses and developmental programs. New Phytol. 2013 Aug 7;199(3):639–49. - 118.
Kazan K, Manners JM. MYC2: the master in action. Mol Plant. 2013 May;6(3):686–703. - 119.
Zander M, Thurow C, Gatz C. TGA Transcription Factors Activate the Salicylic Acid-Suppressible Branch of the Ethylene-Induced Defense Program by Regulating ORA59 Expression. Plant Physiol. 2014 Jul 2;165(4):1671–83. - 120.
Chang C, Yu D, Jiao J, Jing S, Schulze-Lefert P, Shen Q-H. Barley MLA immune receptors directly interfere with antagonistically acting transcription factors to initiate disease resistance signaling. Plant Cell. 2013 Mar;25(3):1158–73. - 121.
Williams SJ, Sohn KH, Wan L, Bernoux M, Sarris PF, Segonzac C, et al. Structural basis for assembly and function of a heterodimeric plant immune receptor. Science. 2014 Apr 18;344(6181):299–303. - 122.
Padmanabhan MS, Ma S, Burch-Smith TM, Czymmek K, Huijser P, Dinesh-Kumar SP. Novel positive regulatory role for the SPL6 transcription factor in the N TIR-NB-LRR receptor-mediated plant innate immunity. PLoS Pathog. 2013 Mar;9(3):e1003235. - 123.
Inoue H, Hayashi N, Matsushita A, Xinqiong L, Nakayama A, Sugano S, et al. Blast resistance of CC-NB-LRR protein Pb1 is mediated by WRKY45 through protein-protein interaction. Proc Natl Acad Sci U S A. 2013 Jun 4;110(23):9577–82. - 124.
Ishihama N, Yoshioka H. Post-translational regulation of WRKY transcription factors in plant immunity. Curr Opin Plant Biol. 2012 Aug;15(4):431–7. - 125.
Ishihama N, Yamada R, Yoshioka M, Katou S, Yoshioka H. Phosphorylation of the Nicotiana benthamiana WRKY8 transcription factor by MAPK functions in the defense response. Plant Cell. 2011 Mar;23(3):1153–70. - 126.
Meng X, Xu J, He Y, Yang K-Y, Mordorski B, Liu Y, et al. Phosphorylation of an ERF transcription factor by Arabidopsis MPK3/MPK6 regulates plant defense gene induction and fungal resistance. Plant Cell. 2013 Mar;25(3):1126–42. - 127.
Pecher P, Eschen-Lippold L, Herklotz S, Kuhle K, Naumann K, Bethke G, et al. The Arabidopsis thaliana mitogen-activated protein kinases MPK3 and MPK6 target a subclass of “VQ-motif”-containing proteins to regulate immune responses. New Phytol. 2014 Jul;203(2):592–606. - 128.
Galon Y, Nave R, Boyce JM, Nachmias D, Knight MR, Fromm H. Calmodulin-binding transcription activator (CAMTA) 3 mediates biotic defense responses in Arabidopsis . FEBS Lett. 2008 Mar 19;582(6):943–8. - 129.
Du L, Ali GS, Simons KA, Hou J, Yang T, Reddy ASN, et al. Ca2+/calmodulin regulates salicylic-acid-mediated plant immunity. Nature. 2009 Jan 4;457(7233):1154–8. - 130.
Wang L, Tsuda K, Truman W, Sato M, Nguyen L V, Katagiri F, et al. CBP60g and SARD1 play partially redundant critical roles in salicylic acid signaling. Plant J. 2011 Sep;67(6):1029–41. - 131.
Pedrini N, Zhang S, Juárez MP, Keyhani NO. Molecular characterization and expression analysis of a suite of cytochrome P450 enzymes implicated in insect hydrocarbon degradation in the entomopathogenic fungus Beauveria bassiana . Microbiology. 2010 Aug 1;156(Pt 8):2549–57. - 132.
Kim HS, Park HC, Kim KE, Jung MS, Han HJ, Kim SH, et al. A NAC transcription factor and SNI1 cooperatively suppress basal pathogen resistance in Arabidopsis thaliana . Nucleic Acids Res. 2012 Oct;40(18):9182–92. - 133.
Gao X, Chen X, Lin W, Chen S, Lu D, Niu Y, et al. Bifurcation of Arabidopsis NLR immune signaling via Ca2+-dependent protein kinases. PLoS Pathog. 2013 Jan;9(1):e1003127. - 134.
Wathugala DL, Hemsley PA, Moffat CS, Cremelie P, Knight MR, Knight H. The Mediator subunit SFR6/MED16 controls defence gene expression mediated by salicylic acid and jasmonate responsive pathways. New Phytol. 2012 Jul;195(1):217–30. - 135.
Çevik V, Kidd BN, Zhang P, Hill C, Kiddle S, Denby KJ, et al. MEDIATOR25 acts as an integrative hub for the regulation of jasmonate-responsive gene expression in Arabidopsis . Plant Physiol. 2012 Sep;160(1):541–55. - 136.
Berr A, Ménard R, Heitz T, Shen W-H. Chromatin modification and remodelling: a regulatory landscape for the control of Arabidopsis defence responses upon pathogen attack. Cell Microbiol. 2012 Jun;14(6):829–39. - 137.
Kim K-C, Lai Z, Fan B, Chen Z. Arabidopsis WRKY38 and WRKY62 transcription factors interact with histone deacetylase 19 in basal defense. Plant Cell. 2008 Sep;20(9):2357–71. - 138.
Alvarez ME, Nota F, Cambiagno DA. Epigenetic control of plant immunity. Mol Plant Pathol. 2010 Jul;11(4):563–76. - 139.
Marino D, Peeters N, Rivas S. Ubiquitination during plant immune signaling. Plant Physiol. 2012 Sep;160(1):15–27. - 140.
Park HJ, Kim W-Y, Park HC, Lee SY, Bohnert HJ, Yun D-J. SUMO and SUMOylation in plants. Mol Cells. 2011 Oct;32(4):305–16. - 141.
Yang S, Tang F, Zhu H. Alternative splicing in plant immunity. Int J Mol Sci. 2014 Jan;15(6):10424–45. - 142.
Pieterse CMJ, Van der Does D, Zamioudis C, Leon-Reyes A, Van Wees SCM. Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol. 2012 Jan;28:489–521. - 143.
Wildermuth MC, Dewdney J, Wu G, Ausubel FM. Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature. 2001 Nov 29;414(6863):562–5. - 144.
Serrano M, Wang B, Aryal B, Garcion C, Abou-Mansour E, Heck S, et al. Export of salicylic acid from the chloroplast requires the multidrug and toxin extrusion-like transporter EDS5. Plant Physiol. 2013 Aug;162(4):1815–21. - 145.
Zhang Y, Xu S, Ding P, Wang D, Cheng YT, He J, et al. Control of salicylic acid synthesis and systemic acquired resistance by two members of a plant-specific family of transcription factors. Proc Natl Acad Sci U S A. 2010 Oct 19;107(42):18220–5. - 146.
Zhang Y, Fan W, Kinkema M, Li X, Dong X. Interaction of NPR1 with basic leucine zipper protein transcription factors that bind sequences required for salicylic acid induction of the PR-1 gene. Proc Natl Acad Sci U S A. 1999 May 25;96(11):6523–8. - 147.
Pajerowska-Mukhtar KM, Emerine DK, Mukhtar MS. Tell me more: roles of NPRs in plant immunity. Trends Plant Sci. 2013 Jul;18(7):402–11. - 148.
Tada Y, Spoel SH, Pajerowska-Mukhtar K, Mou Z, Song J, Wang C, et al. Plant immunity requires conformational changes [corrected] of NPR1 via S-nitrosylation and thioredoxins. Science. 2008 Aug 15;321(5891):952–6. - 149.
Fu ZQ, Yan S, Saleh A, Wang W, Ruble J, Oka N, et al. NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants. Nature. 2012 Jun 14;486(7402):228–32. - 150.
Yan S, Dong X. Perception of the plant immune signal salicylic acid. Curr Opin Plant Biol. 2014 Aug;20:64–8. - 151.
Kazan K, Manners JM. Jasmonate signaling: toward an integrated view. Plant Physiol. 2008 Apr 1;146(4):1459–68. - 152.
Chini A, Fonseca S, Fernández G, Adie B, Chico JM, Lorenzo O, et al. The JAZ family of repressors is the missing link in jasmonate signalling. Nature. 2007 Aug 9;448(7154):666–71. - 153.
Kazan K, Manners JM. JAZ repressors and the orchestration of phytohormone crosstalk. Trends Plant Sci. 2012 Jan;17(1):22–31. - 154.
Lyons R, Manners JM, Kazan K. Jasmonate biosynthesis and signaling in monocots: a comparative overview. Plant Cell Rep. 2013 Jun;32(6):815–27. - 155.
Antico CJ, Colon C, Banks T, Ramonell KM. Insights into the role of jasmonic acid-mediated defenses against necrotrophic and biotrophic fungal pathogens. Front Biol (Beijing). 2012 Jan 8;7(1):48–56. - 156.
Kazan K, Lyons R. Intervention of Phytohormone Pathways by Pathogen Effectors. Plant Cell. 2014 Jun 10;26(6):2285–309. - 157.
Wang KL-C, Li H, Ecker JR. Ethylene biosynthesis and signaling networks. Plant Cell. 2002 Jan;14 Suppl:S131–51. - 158.
Li G, Meng X, Wang R, Mao G, Han L, Liu Y, et al. Dual-level regulation of ACC synthase activity by MPK3/MPK6 cascade and its downstream WRKY transcription factor during ethylene induction in Arabidopsis . PLoS Genet. 2012 Jun;8(6):e1002767. - 159.
Ju C, Yoon GM, Shemansky JM, Lin DY, Ying ZI, Chang J, et al. CTR1 phosphorylates the central regulator EIN2 to control ethylene hormone signaling from the ER membrane to the nucleus in Arabidopsis . Proc Natl Acad Sci U S A. 2012 Nov 20;109(47):19486–91. - 160.
Wen X, Zhang C, Ji Y, Zhao Q, He W, An F, et al. Activation of ethylene signaling is mediated by nuclear translocation of the cleaved EIN2 carboxyl terminus. Cell Res. 2012 Nov;22(11):1613–6. - 161.
Zander M, Chen S, Imkampe J, Thurow C, Gatz C. Repression of the Arabidopsis thaliana jasmonic acid/ethylene-induced defense pathway by TGA-interacting glutaredoxins depends on their C-terminal ALWL motif. Mol Plant. 2012 Jul;5(4):831–40. - 162.
Qiao H, Shen Z, Huang SC, Schmitz RJ, Urich MA, Briggs SP, et al. Processing and subcellular trafficking of ER-tethered EIN2 control response to ethylene gas. Science. 2012 Oct 19;338(6105):390–3. - 163.
De Vleesschauwer D, Xu J, Höfte M. Making sense of hormone-mediated defense networking: from rice to Arabidopsis . Front Plant Sci. 2014 Jan;5:611. - 164.
Caarls L, Pieterse CMJ, Van Wees SCM. How salicylic acid takes transcriptional control over jasmonic acid signaling. Front Plant Sci. 2015 Jan;6:170. - 165.
Song S, Huang H, Gao H, Wang J, Wu D, Liu X, et al. Interaction between MYC2 and ETHYLENE INSENSITIVE3 modulates antagonism between jasmonate and ethylene signaling in Arabidopsis . Plant Cell. 2014 Jan;26(1):263–79. - 166.
Segonzac C, Macho AP, Sanmartín M, Ntoukakis V, Sánchez-Serrano JJ, Zipfel C. Negative control of BAK1 by protein phosphatase 2A during plant innate immunity. EMBO J. 2014 Sep 17;33(18):2069–79. - 167.
Anderson JC, Bartels S, González Besteiro MA, Shahollari B, Ulm R, Peck SC. Arabidopsis MAP Kinase Phosphatase 1 (AtMKP1) negatively regulates MPK6-mediated PAMP responses and resistance against bacteria. Plant J. 2011 Jul;67(2):258–68. - 168.
Lu D, Lin W, Gao X, Wu S, Cheng C, Avila J, et al. Direct ubiquitination of pattern recognition receptor FLS2 attenuates plant innate immunity. Science. 2011 Jun 17;332(6036):1439–42. - 169.
Nathalie Leborgne-Castel, Bouhidel K. Plasma membrane protein trafficking in plant-microbe interactions: a plant cell point of view. Front Plant Sci. Frontiers; 2014 Jan 22;5:735. - 170.
Robatzek S, Chinchilla D, Boller T. Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis . Genes Dev. 2006 Mar 1;20(5):537–42. - 171.
Smith JM, Salamango DJ, Leslie ME, Collins CA, Heese A. Sensitivity to Flg22 is modulated by ligand-induced degradation and de novo synthesis of the endogenous flagellin-receptor FLAGELLIN-SENSING2. Plant Physiol. 2014 Jan;164(1):440–54. - 172.
Millet YA, Danna CH, Clay NK, Songnuan W, Simon MD, Werck-Reichhart D, et al. Innate immune responses activated in Arabidopsis roots by microbe-associated molecular patterns. Plant Cell. 2010 Mar;22(3):973–90. - 173.
Faulkner C, Robatzek S. Plants and pathogens: putting infection strategies and defence mechanisms on the map. Curr Opin Plant Biol. 2012 Dec;15(6):699–707. - 174.
Beck M, Wyrsch I, Strutt J, Wimalasekera R, Webb A, Boller T, et al. Expression patterns of flagellin sensing 2 map to bacterial entry sites in plant shoots and roots. J Exp Bot. 2014 Dec;65(22):6487–98. - 175.
Kawchuk LM, Hachey J, Lynch DR, Kulcsar F, van Rooijen G, Waterer DR, et al. Tomato Ve disease resistance genes encode cell surface-like receptors. Proc Natl Acad Sci U S A. 2001;98(11):6511–5. - 176.
Fradin EF, Zhang Z, Rovenich H, Song Y, Liebrand TWH, Masini L, et al. Functional analysis of the tomato immune receptor Ve1 through domain swaps with its non-functional homolog Ve2. PLoS One. 2014 Jan;9(2):e88208. - 177.
Fradin EF, Zhang Z, Juarez Ayala JC, Castroverde CDM, Nazar RN, Robb J, et al. Genetic Dissection of Verticillium Wilt Resistance Mediated by Tomato Ve1. Plant Physiol. 2009;150(1):320–32. - 178.
Fradin EF, Abd-El-Haliem A, Masini L, van den Berg GCM, Joosten MHAJ, Thomma BPHJ. Interfamily Transfer of Tomato Ve1 Mediates Verticillium Resistance inArabidopsis . Plant Physiol. 2011;156(4):2255–65. - 179.
Zhang Z, Fradin E, de Jonge R, van Esse HP, Smit P, Liu C-M, et al. Optimized agroinfiltration and virus-induced gene silencing to study Ve1-mediated Verticillium resistance in tobacco. Mol Plant Microbe Interact. 2013 Mar;26(2):182–90. - 180.
De Jonge R, van Esse HP, Maruthachalam K, Bolton MD, Santhanam P, Saber MK, et al. Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing. Proc Natl Acad Sci. National Acad Sciences; 2012;109(13):5110–5. - 181.
Liebrand TWH, van den Berg GCM, Zhang Z, Smit P, Cordewener JHG, America AHP, et al. Receptor-like kinase SOBIR1/EVR interacts with receptor-like proteins in plant immunity against fungal infection. Proc Natl Acad Sci U S A. 2013 Jun 11;110(24):10010–5. - 182.
Liebrand TWH, van den Burg HA, Joosten MHAJ. Two for all: receptor-associated kinases SOBIR1 and BAK1. Trends Plant Sci. 2014 Feb;19(2):123–32. - 183.
Liebrand TWH, Kombrink A, Zhang Z, Sklenar J, Jones AME, Robatzek S, et al. Chaperones of the endoplasmic reticulum are required for Ve1-mediated resistance to Verticillium . Mol Plant Pathol. 2014 Jan;15(1):109–17. - 184.
Huang C-C, Lindhout P. Screening for resistance in wild Lycopersicon species toFusarium oxysporum f.sp.lycopersici race 1 and race 2. Euphytica. Kluwer Academic Publishers; 93(2):145–53. - 185.
Beckman CH. Phenolic-storing cells: keys to programmed cell death and periderm formation in wilt disease resistance and in general defence responses in plants? Physiol Mol Plant Pathol. 2000 Sep;57(3):101–10. - 186.
Houterman PM, Ma L, van Ooijen G, de Vroomen MJ, Cornelissen BJC, Takken FLW, et al. The effector protein Avr2 of the xylem-colonizing fungus Fusarium oxysporum activates the tomato resistance protein I-2 intracellularly. Plant J. 2009 Jul;58(6):970–8. - 187.
Michielse CB, van Wijk R, Reijnen L, Cornelissen BJC, Rep M. Insight into the molecular requirements for pathogenicity of Fusarium oxysporum f. sp. lycopersici through large-scale insertional mutagenesis. Genome Biol. 2009 Jan;10(1):R4. - 188.
Ma L, Cornelissen BJC, Takken FLW. A nuclear localization for Avr2 from Fusarium oxysporum is required to activate the tomato resistance protein I-2. Front Plant Sci. 2013 Jan;4:94. - 189.
Gawehns F, Houterman PM, Ichou FA, Michielse CB, Hijdra M, Cornelissen BJC, et al. The Fusarium oxysporum effector Six6 contributes to virulence and suppresses I-2-mediated cell death. Mol Plant Microbe Interact. The American Phytopathological Society; 2014 May 4;27(4):336–48. - 190.
Ma L, Houterman PM, Gawehns F, Cao L, Sillo F, Richter H, et al. The AVR2-SIX5 gene pair is required to activate I-2-mediated immunity in tomato. New Phytol. 2015 May 13. - 191.
Song WY, Wang GL, Chen LL, Kim HS, Pi LY, Holsten T, et al. A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science. 1995 Dec 15;270(5243):1804–6. - 192.
Lee S-W, Han S-W, Sririyanum M, Park C-J, Seo Y-S, Ronald PC. A type I-secreted, sulfated peptide triggers XA21-mediated innate immunity. Science. 2009 Dec 6;326(5954):850–3. - 193.
Park C-J, Han S-W, Chen X, Ronald PC. Elucidation of XA21-mediated innate immunity. Cell Microbiol. 2010 Aug;12(8):1017–25. - 194.
Chen X, Chern M, Canlas PE, Ruan D, Jiang C, Ronald PC. An ATPase promotes autophosphorylation of the pattern recognition receptor XA21 and inhibits XA21-mediated immunity. Proc Natl Acad Sci U S A. 2010 May 27;107(17):8029–34. - 195.
Park C-J, Peng Y, Chen X, Dardick C, Ruan D, Bart R, et al. Rice XB15, a protein phosphatase 2C, negatively regulates cell death and XA21-mediated innate immunity. PLoS Biol. 2008 Oct 23;6(9):e231. - 196.
Wang Y-S, Pi L-Y, Chen X, Chakrabarty PK, Jiang J, De Leon AL, et al. Rice XA21 binding protein 3 is a ubiquitin ligase required for full Xa21-mediated disease resistance. Plant Cell. 2006 Dec;18(12):3635–46. - 197.
Jiang Y, Chen X, Ding X, Wang Y, Chen Q, Song W-Y. The XA21 binding protein XB25 is required for maintaining XA21-mediated disease resistance. Plant J. 2013 Mar;73(5):814–23. - 198.
Peng Y, Bartley LE, Chen X, Dardick C, Chern M, Ruan R, et al. OsWRKY62 is a negative regulator of basal and Xa21-mediated defense against Xanthomonas oryzae pv.oryzae in rice. Mol Plant. 2008 May;1(3):446–58. - 199.
Park C-J, Bart R, Chern M, Canlas PE, Bai W, Ronald PC. Overexpression of the endoplasmic reticulum chaperone BiP3 regulates XA21-mediated innate immunity in rice. PLoS One. 2010 Jan;5(2):e9262. - 200.
Narusaka M, Shirasu K, Noutoshi Y, Kubo Y, Shiraishi T, Iwabuchi M, et al. RRS1 and RPS4 provide a dual Resistance-gene system against fungal and bacterial pathogens. Plant J. 2009 Oct;60(2):218–26. - 201.
Narusaka M, Hatakeyama K, Shirasu K, Narusaka Y. Arabidopsis dual resistance proteins, both RPS4 and RRS1, are required for resistance to bacterial wilt in transgenicBrassica crops. Plant Signal Behav. 2014 Jan;9(7):e29130. - 202.
Saucet SB, Ma Y, Sarris PF, Furzer OJ, Sohn KH, Jones JDG. Two linked pairs of Arabidopsis TNL resistance genes independently confer recognition of bacterial effector AvrRps4. Nat Commun. 2015 Jan;6:6338. - 203.
Deslandes L, Olivier J, Theulieres F, Hirsch J, Feng DX, Bittner-Eddy P, et al. Resistance to Ralstonia solanacearum inArabidopsis thaliana is conferred by the recessive RRS1-R gene, a member of a novel family of resistance genes. Proc Natl Acad Sci U S A. 2002 Mar 19;99(4):2404–9. - 204.
Deslandes L, Olivier J, Peeters N, Feng DX, Khounlotham M, Boucher C, et al. Physical interaction between RRS1-R, a protein conferring resistance to bacterial wilt, and PopP2, a type III effector targeted to the plant nucleus. Proc Natl Acad Sci U S A. 2003 Jul 24;100(13):8024–9. - 205.
Sarris PF, Duxbury Z, Huh SU, Ma Y, Segonzac C, Sklenar J, et al. A Plant Immune Receptor Detects Pathogen Effectors that Target WRKY Transcription Factors. Cell. 2015 May 21;161(5):1089–100. - 206.
Le Roux C, Huet G, Jauneau A, Camborde L, Trémousaygue D, Kraut A, et al. A Receptor Pair with an Integrated Decoy Converts Pathogen Disabling of Transcription Factors to Immunity. Cell. 2015 May 21;161(5):1074–88. - 207.
Reusche M, Thole K, Janz D, Truskina J, Rindfleisch S, Drübert C, et al. Verticillium infection triggers VASCULAR-RELATED NAC DOMAIN7-dependent de novo xylem formation and enhances drought tolerance inArabidopsis . Plant Cell. 2012 Sep;24(9):3823–37. - 208.
Hu J, Barlet X, Deslandes L, Hirsch J, Feng DX, Somssich I, et al. Transcriptional responses of Arabidopsis thaliana during wilt disease caused by the soil-borne phytopathogenic bacterium,Ralstonia solanacearum . PLoS One. 2008 Jan;3(7):e2589. - 209.
Zhang Y, Wang XF, Ding ZG, Ma Q, Zhang GR, Zhang SL, et al. Transcriptome profiling of Gossypium barbadense inoculated withVerticillium dahliae provides a resource for cotton improvement. BMC Genomics. BioMed Central Ltd; 2013;14(1):637. - 210.
Van Esse HP, Fradin EF, de Groot PJ, de Wit PJGM, Thomma BPHJ. Tomato transcriptional responses to a foliar and a vascular fungal pathogen are distinct. Mol Plant Microbe Interact. 2009 Mar;22(3):245–58. - 211.
Chen YC, Wong CL, Muzzi F, Vlaardingerbroek I, Kidd BN, Schenk PM. Root defense analysis against Fusarium oxysporum reveals new regulators to confer resistance. Sci Rep. Nature Publishing Group; 2014 Jan 7;4:5584. - 212.
Robb J, Shittu H, Soman K V, Kurosky A, Nazar RN. Arsenal of elevated defense proteins fails to protect tomato against Verticillium dahliae . Planta. 2012;236(2):623–33. - 213.
Mandelc S, Timperman I, Radišek S, Devreese B, Samyn B, Javornik B. Comparative proteomic profiling in compatible and incompatible interactions between hop roots and Verticillium albo-atrum . Plant Physiol Biochem. 2013 Jul;68:23–31. - 214.
Sestili S, Polverari A, Luongo L, Ferrarini A, Scotton M, Hussain J, et al. Distinct colonization patterns and cDNA-AFLP transcriptome profiles in compatible and incompatible interactions between melon and different races of Fusarium oxysporum f. sp.melonis . BMC Genomics. 2011 Jan;12:122.