Cytokinins and plant immunity: old foes or new friends?
2011; Elsevier BV; Volume: 16; Issue: 7 Linguagem: Inglês
10.1016/j.tplants.2011.03.003
ISSN1878-4372
AutoresJaemyung Choi, Daeseok Choi, Seung‐Chul Lee, Choong‐Min Ryu, Ildoo Hwang,
Tópico(s)Plant Parasitism and Resistance
ResumoCytokinins are plant growth promoting hormones involved in the specification of embryonic cells, maintenance of meristematic cells, shoot formation and development of vasculature. Cytokinins have also emerged as a major factor in plant–microbe interactions during nodule organogenesis and pathogenesis. Microbe-originated cytokinins confer abnormal hypersensitivity of cytokinins to plants, augmenting the sink activity of infected regions. However, recent findings have shed light on a distinct role of cytokinins in plant immune responses. Plant-borne cytokinins systemically induce resistance against pathogen infection. This resistance is orchestrated by endogenous cytokinin and salicylic acid signaling. Here, we discuss how plant- and pathogen-derived cytokinins inversely affect the plant defense response. In addition, we consider the molecular mechanisms underlying plant-derived cytokinin action in plant immunity. Cytokinins are plant growth promoting hormones involved in the specification of embryonic cells, maintenance of meristematic cells, shoot formation and development of vasculature. Cytokinins have also emerged as a major factor in plant–microbe interactions during nodule organogenesis and pathogenesis. Microbe-originated cytokinins confer abnormal hypersensitivity of cytokinins to plants, augmenting the sink activity of infected regions. However, recent findings have shed light on a distinct role of cytokinins in plant immune responses. Plant-borne cytokinins systemically induce resistance against pathogen infection. This resistance is orchestrated by endogenous cytokinin and salicylic acid signaling. Here, we discuss how plant- and pathogen-derived cytokinins inversely affect the plant defense response. In addition, we consider the molecular mechanisms underlying plant-derived cytokinin action in plant immunity. Cytokinins are growth control hormones, which promote cell division, nutrient mobilization and leaf longevity [1Choi J. Hwang I. Cytokinin: perception, signal transduction, and role in plant growth and development.J. Plant Biol. 2007; 50: 98-108Crossref Scopus (47) Google Scholar, 2Kim H.J. et al.Cytokinin-mediated control of leaf longevity by AHK3 through phosphorylation of ARR2 in Arabidopsis.Proc. Natl. Acad. Sci. U.S.A. 2006; 103: 814-819Crossref PubMed Scopus (333) Google Scholar, 3Matsumoto-Kitano M. et al.Cytokinins are central regulators of cambial activity.Proc. Natl. Acad. Sci. U.S.A. 2008; 105: 20027-20031Crossref PubMed Scopus (277) Google Scholar, 4Sakakibara H. Cytokinins: activity, biosynthesis, and translocation.Annu. Rev. 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Cytokinins can also increase grain yield; for example, by activating inflorescence meristem activity in rice (Oryza sativa) [9Kurakawa T. et al.Direct control of shoot meristem activity by a cytokinin-activating enzyme.Nature. 2007; 445: 652-655Crossref PubMed Scopus (615) Google Scholar, 10Ashikari M. et al.Cytokinin oxidase regulates rice grain production.Science. 2005; 309: 741-745Crossref PubMed Scopus (1245) Google Scholar]. Moreover, cytokinin accumulation in tobacco (Nicotiana tabacum) leads to tolerance against extreme drought stress [11Rivero R.M. et al.Delayed leaf senescence induces extreme drought tolerance in a flowering plant.Proc. Natl. Acad. Sci. U.S.A. 2007; 104: 19631-19636Crossref PubMed Scopus (632) Google Scholar]. These features highlight the importance of cytokinins in agricultural applications. However, many microbes, mostly plant pathogens, also secrete cytokinin analogs or activate plant cytokinin production to divert nutrients from the host toward dedicated growth of infected tissues, which results in a loss of productivity in agricultural crops [12Robert-Seilaniantz A. et al.Pathological hormone imbalances.Curr. Opin. Plant Biol. 2007; 10: 372-379Crossref PubMed Scopus (428) Google Scholar, 13Walters D.R. McRoberts N. Plants and biotrophs: a pivotal role for cytokinins?.Trends Plant Sci. 2006; 11: 581-586Abstract Full Text Full Text PDF PubMed Scopus (159) Google Scholar, 14Walters D.R. et al.Are green islands red herrings? Significance of green islands in plant interactions with pathogens and pests.Biol. Rev. Camb. Philos. Soc. 2008; 83: 79-102Crossref PubMed Scopus (96) Google Scholar, 15Pertry I. et al.Rhodococcus fascians impacts plant development through the dynamic Fas-mediated production of a cytokinin mix.Mol. 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It has been assumed that the cytokinin-mediated growth response suppresses plant basal defense mechanisms [12Robert-Seilaniantz A. et al.Pathological hormone imbalances.Curr. Opin. Plant Biol. 2007; 10: 372-379Crossref PubMed Scopus (428) Google Scholar]; however, recent work has revealed that plant-originated cytokinins augment plant immunity together with salicylic acid (SA) signaling [17Choi J. et al.The cytokinin-activated transcription factor ARR2 promotes plant immunity via TGA3/NPR1-dependent salicylic acid signaling in Arabidopsis.Dev. Cell. 2010; 19: 284-295Abstract Full Text Full Text PDF PubMed Scopus (263) Google Scholar]. In this review, we discuss the molecular mechanisms underlying distinct actions of plant- and pathogen-derived cytokinins in plant responses, and the role of cytokinins in the priming of plant innate immunity. Gall-forming plant pathogenic bacteria such as Rhodococcus fascians and Agrobacterium tumefaciens and biotrophic fungi such as Puccinia striiformis produce auxin and cytokinins to enhance their pathogenicity and modulate the physiology of host plants [12Robert-Seilaniantz A. et al.Pathological hormone imbalances.Curr. Opin. Plant Biol. 2007; 10: 372-379Crossref PubMed Scopus (428) Google Scholar, 14Walters D.R. et al.Are green islands red herrings? Significance of green islands in plant interactions with pathogens and pests.Biol. Rev. Camb. Philos. Soc. 2008; 83: 79-102Crossref PubMed Scopus (96) Google Scholar, 15Pertry I. et al.Rhodococcus fascians impacts plant development through the dynamic Fas-mediated production of a cytokinin mix.Mol. Plant-Microbe Interact. 2010; 23: 1164-1174Crossref PubMed Scopus (68) Google Scholar, 18Lee C.-W. et al.Agrobacterium tumefaciens promotes tumor induction by modulating pathogen defense in Arabidopsis thaliana.The Plant Cell. 2009; 21: 2948-2962Crossref PubMed Scopus (114) Google Scholar]. R. fascians and A. tumefaciens induce leafy galls and crown galls, respectively. These hyperplasia originate from the abnormal localized accumulation in plant tissues of cytokinins and auxins inducing abnormal cell proliferation and/or delaying the senescence of infected regions to enhance sink activity [15Pertry I. et al.Rhodococcus fascians impacts plant development through the dynamic Fas-mediated production of a cytokinin mix.Mol. Plant-Microbe Interact. 2010; 23: 1164-1174Crossref PubMed Scopus (68) Google Scholar, 16Pertry I. et al.Identification of Rhodococcus fascians cytokinins and their modus operandi to reshape the plant.Proc. Natl. Acad. Sci. 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However, bacterial cytokinins might not be essential for the infection of A. tumefaciens, as both virulent and avirulent strains produce similar quantities of cytokinins in vitro culture [22Jameson P. Cytokinins and auxins in plant-pathogen interactions – An overview.Plant Growth Regul. 2000; 32: 369-380Crossref Scopus (135) Google Scholar]. R. fascians induces abnormal hyper-activation of host cytokinin signaling and confers high cytokinin susceptibility on host plants (Figure 1) [16Pertry I. et al.Identification of Rhodococcus fascians cytokinins and their modus operandi to reshape the plant.Proc. Natl. Acad. Sci. U.S.A. 2009; 106: 929-934Crossref PubMed Scopus (142) Google Scholar, 19Depuydt S. et al.Modulation of the hormone setting by Rhodococcus fascians results in ectopic KNOX activation in Arabidopsis.Plant Physiol. 2008; 146: 1267-1281Crossref PubMed Scopus (41) Google Scholar]. Depending on the host, various types of cytokinins, such as isopentenyladenine (iP), cis-zeatin (cZ), and 2-methylthio-cis-zeatin (2MeScZ), accumulate in R. fascians-infected tissues [16Pertry I. et al.Identification of Rhodococcus fascians cytokinins and their modus operandi to reshape the plant.Proc. Natl. Acad. Sci. U.S.A. 2009; 106: 929-934Crossref PubMed Scopus (142) Google Scholar]. R. fascians itself produces at least six cytokinin bases: cis-zeatin, iP, trans-zeatin (tZ) and their methylthio-derivatives [15Pertry I. et al.Rhodococcus fascians impacts plant development through the dynamic Fas-mediated production of a cytokinin mix.Mol. Plant-Microbe Interact. 2010; 23: 1164-1174Crossref PubMed Scopus (68) Google Scholar]. In Arabidopsis thaliana, pathogen-derived cZ and 2MeScZ are not fully degraded by plant CKXs (see Glossary) and are maintained at high concentrations as long as 35 days after challenged, when the leafy gall is fully developed [16Pertry I. et al.Identification of Rhodococcus fascians cytokinins and their modus operandi to reshape the plant.Proc. Natl. Acad. Sci. U.S.A. 2009; 106: 929-934Crossref PubMed Scopus (142) Google Scholar]. Expression of a cytokinin receptor AHK4 in plants was highly induced by R. fascians infection, which can enhance cytokinin sensitivity of host plants. Genetic analysis showed that of the double cytokinin receptor knockout mutants only ahk3 ahk4 plants failed to induce pathogen-dependent deformations. Accordingly, R. fascians-derived cytokinins recognized mainly by AHK3 and AHK4 appear to be major regulators of plant sensitivity to R. fascians. It is noteworthy that exogenous application of cytokinin mixtures results in a stronger activation of plant cytokinin signaling compared to the application of a single cytokinin species. Each cytokinin has a different binding affinity for the AHK receptors, therefore the mixture of cytokinins produced by the pathogen should be able to simultaneously and synergistically hyper-activate cytokinin responses downstream of AHK3 and AHK4 which results in responsiveness to R. fascians. One of these responses is the induction of KNOX genes including KNAT1 [19Depuydt S. et al.Modulation of the hormone setting by Rhodococcus fascians results in ectopic KNOX activation in Arabidopsis.Plant Physiol. 2008; 146: 1267-1281Crossref PubMed Scopus (41) Google Scholar]. Ectopic expression of KNAT1 results in aberrant cell divisions in leaves, which causes leaf serrations, a typical symptom of R. fascians infection. Such leaf deformations can be partially mimicked by a high dose of exogenous cytokinin, indicating R. fascians might induce pathological symptoms by cytokinins via KNOX. Although KNOX proteins induce cytokinin biosynthetic IPT genes in normal conditions [23Yanai O. et al.Arabidopsis KNOXI proteins activate cytokinin biosynthesis.Curr. Biol. 2005; 15: 1566-1571Abstract Full Text Full Text PDF PubMed Scopus (373) Google Scholar, 24Jasinski S. et al.KNOX action in Arabidopsis is mediated by coordinate regulation of cytokinin and gibberellin activities.Curr. Biol. 2005; 15: 1560-1565Abstract Full Text Full Text PDF PubMed Scopus (496) Google Scholar], R. fascians-induced KNOX proteins fail to induce plant cytokinin production, because IPT genes are downregulated during R. fascians infection, rather than induced [25Depuydt S. et al.An integrated genomics approach to define niche establishment by Rhodococcus fascians.Plant Physiol. 2009; 149: 1366-1386Crossref PubMed Scopus (64) Google Scholar]. Recently, the effect of R. fascians infection on the plant transcriptome has been studied extensively [25Depuydt S. et al.An integrated genomics approach to define niche establishment by Rhodococcus fascians.Plant Physiol. 2009; 149: 1366-1386Crossref PubMed Scopus (64) Google Scholar]. As R. fascians-derived cytokinins play a critical role in its pathogenicity, cytokinin-inducible cell wall-loosening expansins involved in cell proliferation were induced upon R. fascians infection [25Depuydt S. et al.An integrated genomics approach to define niche establishment by Rhodococcus fascians.Plant Physiol. 2009; 149: 1366-1386Crossref PubMed Scopus (64) Google Scholar]. Surprisingly, the expression of cytokinin-induced ROS producers, scavengers and antioxidants, which are critical for stress and defense responses, was reduced by R. fascians. For this reason, it is likely that R. fascians can activate complex crosstalking of cytokinin-regulated growth responses while suppressing cytokinin-induced defense responses. The same set of cytokinin-induced stress and defense-related genes is also suppressed by auxin secreted from A. tumefaciens, which employs auxin for pathogenicity and crown-gall formation [18Lee C.-W. et al.Agrobacterium tumefaciens promotes tumor induction by modulating pathogen defense in Arabidopsis thaliana.The Plant Cell. 2009; 21: 2948-2962Crossref PubMed Scopus (114) Google Scholar], thus suggesting that pathogen-derived auxin specifically suppresses the cytokinin-induced defense response during infection (Figure 1). In contrast to the cytokinins produced by many biotrophic bacterial and fungal pathogens for their proliferation in host plants, plant-derived cytokinins can be involved in plant resistance to viral infection [26Masuta C. et al.Broad resistance to plant viruses in transgenic plants conferred by antisense inhibition of a host gene essential in S-adenosylmethionine-dependent transmethylation reactions.Proc. Natl. Acad. Sci. 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However, the molecular mechanisms of cytokinin action in disease resistance to a wide spectrum of pathogens and the reason for the inverse effects of cytokinins on plant responses against biotrophic pathogens and viral infection have remained elusive. S-ADENOSYLHOMOCYSTEINE HYDROLASE (SAHH) mediates intracellular conversion of S-adenoslhomocysteine (SAH) to S-adenosylmethionine (SAM) [26Masuta C. et al.Broad resistance to plant viruses in transgenic plants conferred by antisense inhibition of a host gene essential in S-adenosylmethionine-dependent transmethylation reactions.Proc. Natl. Acad. Sci. U.S.A. 1995; 92: 6117-6121Crossref PubMed Scopus (73) Google Scholar]. Because SAHH could mediate the methylation of the 5′-terminus of viral mRNA, which is a prerequisite for viral replication, antisense inhibition of SAHH is used to suppress viral infection in tobacco plants. The transgenic plants exhibit broad local and systemic resistance to various viruses, including tobacco mosaic virus (TMV), cucumber mosaic virus (CMV), and potato virus X (PVX). It is particularly interesting that these plants also show enhanced resistance to potato virus Y (PVY), which does not require the methylated cap structure for replication. Unexpectedly, about half of the transgenic plants show slightly stunted growth, and root exudates of the transgenic plants contain three times the amount of endogenous cytokinins measured in wild-type plants. These results suggest that the increased cytokinins in the transgenic plants, rather than the direct suppression of viral mRNA cap methylation, are indirectly related to their enhanced resistance to PVY. Similarly, the rice rgpl transgenic tobacco plants have enhanced resistance to TMV infection after wound treatment. In rice, rgpl is a Rab/Ypt-related small GTP-binding protein [28Sano H. et al.Expression of the gene for a small GTP binding protein in transgenic tobacco elevates endogenous cytokinin levels, abnormally induces salicylic acid in response to wounding, and increases resistance to tobacco mosaic virus infection.Proc. Natl. Acad. Sci. U.S.A. 1994; 91: 10556-10560Crossref PubMed Scopus (138) Google Scholar]. Introduction of the rgpl gene into tobacco results in reduced apical dominance and increased tillering, which is reminiscent of activated cytokinin signaling. Consistent with this finding, the accumulation of endogenous zeatin and zeatin ribose is evident in rgpl transgenic plants. The TMV resistance of the transgenic plant results from the accumulation of SA upon wounding in wounded as well as in unwounded systemic leaves. It is apparent that incompatible biotrophic pathogens trigger SA-mediated defense responses, including the induction of acidic pathogenesis-related (PR) proteins such as PR-1a in tobacco. Although it is not clear whether cytokinins directly induce SA accumulation, these studies imply that plant-derived cytokinin accumulation results in an altered morphology and resistance to viral infection, at least in part, through SA accumulation. Plants possess disease resistance (R) proteins that are able to target avirulent proteins from specified pathogens. The majority of R proteins usually contain a nucleotide-binding (NB) leucine-rich-repeat (LRR) domain with a N-terminal Toll/Interleukin 1 receptor (TIR) region (TIR-NB-LRR) or with a putative coiled-coil region at the N-terminus (CC-NB-LRR) [30Bent A.F. Mackey D. Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions.Annu. Rev. Phytopathol. 2007; 45: 399-436Crossref PubMed Scopus (565) Google Scholar]. These R proteins recognize specific avirulence (avr) effector proteins from pathogens and then trigger a defense response such as SA accumulation, leading to induction of PR genes and systemic acquired resistance (SAR). UNI1 is a CC-NB-LRR protein that could function as an R protein and elicit the SA-dependent signaling pathway [31Uchida N. Tasaka M. Intersections between immune responses and morphological regulation in plants.J. Exp. Biol. 2010; 61: 2539-2547Google Scholar, 32Chung K.-M. et al.New perspectives on plant defense responses through modulation of developmental pathways.Mol. Cells. 2008; 26: 107-112PubMed Google Scholar, 33Igari K. et al.Constitutive activation of a CC-NB-LRR protein alters morphogenesis through the cytokinin pathway in Arabidopsis.Plant J. 2008; 55: 14-27Crossref PubMed Scopus (72) Google Scholar]. 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U.S.A. 2006; 103: 19200-19205Crossref PubMed Scopus (92) Google Scholar]. uni-1D plants exhibit phenotypes typical of activated cytokinin signaling, such as loss of apical dominance with ectopic auxiliary meristem formation, delayed senescence and late flowering [33Igari K. et al.Constitutive activation of a CC-NB-LRR protein alters morphogenesis through the cytokinin pathway in Arabidopsis.Plant J. 2008; 55: 14-27Crossref PubMed Scopus (72) Google Scholar]. In the uni-1D mutant, the expression of cytokinin-responsive type-A ARRs, ARR5 and ARR6, is also induced probably by increased endogenous tZ and its conjugated forms (Figure 2). Cytokinin depletion by CKX1 overexpression in a uni-1D background suppresses the formation of ectopic meristems and, interestingly, abolishes the activation of both ARR5 and PR1. Therefore, it is likely that UNI is involved in both SA signaling and plant development via the modulation of cytokinin levels. RIN4 is degraded by Pseudomonas syringae effectors AvrRpm1 and AvrRpt2 [39Belkhadir Y. et al.Arabidopsis RIN4 negatively regulates disease resistance mediated by RPS2 and RPM1 downstream or independent of the NDR1 signal modulator and is not required for the virulence functions of bacterial type III effectors AvrRpt2 or AvrRpm1.The Plant Cell. 2004; 16: 2822-2835Crossref PubMed Scopus (187) Google Scholar, 40Kim M.G. et al.Two Pseudomonas syringae type III effectors inhibit RIN4-regulated basal defense in Arabidopsis.Cell. 2005; 121: 749-759Abstract Full Text Full Text PDF PubMed Scopus (355) Google Scholar]. Two R proteins, RPS2 and RPM1, recognize the degradation of RIN4 and activate the plant defense response. Activation of RPS2 and RPM1 by RIN4 knockdown also results in the activation of expression of the primary cytokinin-responsive gene ARR5 and in ectopic auxiliary meristem formation [33Igari K. et al.Constitutive activation of a CC-NB-LRR protein alters morphogenesis through the cytokinin pathway in Arabidopsis.Plant J. 2008; 55: 14-27Crossref PubMed Scopus (72) Google Scholar]. Given these findings, it appears that the R protein-mediated defense response employs cytokinin signaling, which augments SA signaling output to reinforce plant immunity. Although interplay between cytokinin and SA in plant immunity has been suggested based on phenotypic and genetic data, the molecular mechanism determining how cytokinins affect SA signaling and plant responses against pathogen attack is unclear. Recently, it has been suggested that cytokinin signaling through AHK2 and AHK3 receptors activates SA signaling during the interaction with P. syringae pv. tomato DC3000 (Pst DC3000), a hemibiotrophic bacterial pathogen that causes bacterial speck in Arabidopsis (Figure 2) [17Choi J. et al.The cytokinin-activated transcription factor ARR2 promotes plant immunity via TGA3/NPR1-dependent salicylic acid signaling in Arabidopsis.Dev. Cell. 2010; 19: 284-295Abstract Full Text Full Text PDF PubMed Scopus (263) Google Scholar]. Exogenous application of tZ or increased endogenous cytokinins in IPT-overexpressing plants enhances plant resistance against Pst DC3000, whereas ahk2 ahk3 double knockout plants enhance susceptibility. Cytokinins transiently induce the transcription of defense-related genes, including an SA biosynthetic gene SID2, a transcription factor WRKY18, and an SA signaling marker gene PR1. As a result, the endogenous SA level is increased after cytokinin treatment. Cytokinin perception initiates a multiple phosphorelay via a two-component signaling cascade, resulting in the phosphorylation of the conserved aspartate residue in ARR transcriptional regulators. ARR2, a type-B ARR that is activated by cytokinins, binds directly to the promoters of PR1 and PR2 to induce their transcription, and its activity is directly correlated with plant resistance to the pathogen. As the non-phosphorylable form of ARR2 fails to induce resistance to Pst DC3000, it seems that cytokinin-dependent phosphorylation of ARR2 is crucial for the expression of defense-related genes. Although ARR2 binds to PR gene promoters, the cytokinin-induced defense response through ARR2 activation depends on SA signaling. The knockout of NPR1 or NahG transgenic plants fails to induce a cytokinin-mediated defense response. It turns out that ARR2 interacts with the SA response factor TGA3 and the application of SA enhances the binding of ARR2 to the PR1 promoter. Because SA accumulation stimulated by the perception of microbe-associated molecular patterns (MAMPs) enhances callose deposition [41Clay N.K. et al.Glucosinolate metabolites required for an Arabidopsis innate immune response.Science. 2009; 323: 95-101Crossref PubMed Scopus (766) Google Scholar], 35S:IPT3 with high endogenous cytokinins and 35S:ARR2 plants exhibit elevated callose deposition upon Pst inoculation. These findings suggest that TGA3 recruits ARR2 to the promoters of defense genes when SA signaling is activated, and cytokinin-dependent phosphorylation of ARR2 induces hyper-activation of their transcription together with SA-dependent TGA3. There are 12 type-B ARRs in Arabidopsis [42Hwang I. et al.Two-component signal transduction pathways in Arabidopsis.Plant Physiol. 2002; 129: 500-515Crossref PubMed Scopus (301) Google Scholar]. 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