RESUMEN
In the presence of pathogenic bacteria, plants close their stomata to prevent pathogen entry. Intracellular nucleotide-binding leucine-rich repeat (NLR) immune receptors recognize pathogenic effectors and activate effector-triggered immune responses. However, the regulatory and molecular mechanisms of stomatal immunity involving NLR immune receptors are unknown. Here, we show that the Nicotiana benthamiana RPW8-NLR central immune receptor ACTIVATED DISEASE RESISTANCE 1 (NbADR1), together with the key immune proteins ENHANCED DISEASE SUSCEPTIBILITY 1 (NbEDS1) and PHYTOALEXIN DEFICIENT 4 (NbPAD4), plays an essential role in bacterial pathogen- and flg22-induced stomatal immunity by regulating the expression of salicylic acid (SA) and abscisic acid (ABA) biosynthesis or response-related genes. NbADR1 recruits NbEDS1 and NbPAD4 in stomata to form a stomatal immune response complex. The transcription factor NbWRKY40e, in association with NbEDS1 and NbPAD4, modulates the expression of SA and ABA biosynthesis or response-related genes to influence stomatal immunity. NbADR1, NbEDS1, and NbPAD4 are required for the pathogen infection-enhanced binding of NbWRKY40e to the ISOCHORISMATE SYNTHASE 1 promoter. Moreover, the ADR1-EDS1-PAD4 module regulates stomatal immunity in Arabidopsis (Arabidopsis thaliana). Collectively, our findings show the pivotal role of the core intracellular immune receptor module ADR1-EDS1-PAD4 in stomatal immunity, which enables plants to limit pathogen entry.
Asunto(s)
Proteínas de Arabidopsis , Arabidopsis , Arabidopsis/metabolismo , Proteínas de Arabidopsis/metabolismo , Nicotiana/genética , Lipasa/metabolismo , Proteínas de Unión al ADN/metabolismo , Hidrolasas de Éster Carboxílico/genética , Inmunidad de la Planta/genética , Enfermedades de las Plantas/microbiologíaRESUMEN
Plant diseases are among the major causes of crop yield losses around the world. To confer disease resistance, conventional breeding relies on the deployment of single resistance (R) genes. However, this strategy has been easily overcome by constantly evolving pathogens. Disabling susceptibility (S) genes is a promising alternative to R genes in breeding programs, as it usually offers durable and broad-spectrum disease resistance. In Arabidopsis, the S gene DMR6 (AtDMR6) encodes an enzyme identified as a susceptibility factor to bacterial and oomycete pathogens. Here, we present a model-to-crop translational work in which we characterize two AtDMR6 orthologs in tomato, SlDMR6-1 and SlDMR6-2. We show that SlDMR6-1, but not SlDMR6-2, is up-regulated by pathogen infection. In agreement, Sldmr6-1 mutants display enhanced resistance against different classes of pathogens, such as bacteria, oomycete, and fungi. Notably, disease resistance correlates with increased salicylic acid (SA) levels and transcriptional activation of immune responses. Furthermore, we demonstrate that SlDMR6-1 and SlDMR6-2 display SA-5 hydroxylase activity, thus contributing to the elucidation of the enzymatic function of DMR6. We then propose that SlDMR6 duplication in tomato resulted in subsequent subfunctionalization, in which SlDMR6-2 specialized in balancing SA levels in flowers/fruits, while SlDMR6-1 conserved the ability to fine-tune SA levels during pathogen infection of the plant vegetative tissues. Overall, this work not only corroborates a mechanism underlying SA homeostasis in plants, but also presents a promising strategy for engineering broad-spectrum and durable disease resistance in crops.
Asunto(s)
Resistencia a la Enfermedad/inmunología , Enfermedades de las Plantas/inmunología , Enfermedades de las Plantas/microbiología , Proteínas de Plantas/metabolismo , Homología de Secuencia de Aminoácido , Solanum lycopersicum/inmunología , Proteínas de Arabidopsis/metabolismo , Biocatálisis , Regulación de la Expresión Génica de las Plantas , Gentisatos/metabolismo , Solanum lycopersicum/genética , Solanum lycopersicum/crecimiento & desarrollo , Mutación/genética , Filogenia , Inmunidad de la Planta/genética , Proteínas de Plantas/genética , Plantas Modificadas Genéticamente , Ácido Salicílico/metabolismo , Transcriptoma/genética , Regulación hacia Arriba , Xanthomonas/fisiologíaRESUMEN
Flower development and fertility are coordinately regulated by endogenous developmental signals, including the phytohormones jasmonates (JAs), auxin, and gibberellin, and environmental cues. JAs regulate stamen development and fertility under basal conditions, affect root growth and trichome formation under stress conditions, and control defense responses against insect herbivores and pathogens. Since the 1990s, an increasing number of studies have revealed the essential roles of JA biosynthesis, signaling, and crosstalk in regulation of flower development and fertility. Here, we summarize and present an updated overview of the JA pathway and its crosstalk in modulating flower/sexual organ development and fertility in Arabidopsis, tomato, rice, maize, and sorghum.
Asunto(s)
Proteínas de Arabidopsis , Arabidopsis , Reguladores del Crecimiento de las Plantas/metabolismo , Giberelinas/metabolismo , Ciclopentanos/metabolismo , Oxilipinas/metabolismo , Fertilidad , Arabidopsis/metabolismo , Proteínas de Arabidopsis/metabolismo , Flores , Regulación de la Expresión Génica de las PlantasRESUMEN
Maize stalk rot, caused by multiple pathogens, is a serious soilborne disease worldwide. Composition of pathogens causing maize stalk rot and resistance of maize inbred lines in Heilongjiang Province, China, are not well understood. In this study, 138 fungal isolates were collected from different maize-producing areas in Heilongjiang Province, which were identified as Fusarium graminearum (23.2%), F. subglutinans (18.9%), F. cerealis (18.9%), Bipolaris zeicola (13.0%), F. brachygibbosum (13.0%), F. temperatum (7.2%), and F. proliferatum (5.8%). Among them, F. graminearum (>20%) was the predominant species among the isolates causing maize stalk rot. B. zeicola had not previously been reported causing maize stalk rot in China. Resistance of 67 maize inbred lines to maize stalk rot was assessed, and 24 lines (35.8% of them) were highly resistant or resistant, indicating that approximately 65% of these lines were susceptible to maize stalk rot. Maize inbred lines were analyzed using simple sequence repeat markers and divided into five genetic groups with 12 pairs of primers. Additionally, analysis of molecular variance indicated that 44.2% of the genetic variation in disease resistance was distributed among populations. This study provides insight into the genetic diversity of inbred maize and may contribute useful information for breeding stalk rot disease-resistant hybrids, and facilitates development of effective strategies for managing this destructive disease complex.
Asunto(s)
Enfermedades de las Plantas , Zea mays , Zea mays/genética , Zea mays/microbiología , Enfermedades de las Plantas/microbiología , Fitomejoramiento , China , Variación GenéticaRESUMEN
The phytohormones jasmonates (JAs) control plant development, growth, and defense against insects and pathogens. The Arabidopsis JA receptor Coronatine Insensitive 1 (COI1) interacts with ARABIDOPSIS SKP-LIKE1 (ASK1)/ASK2 to form the SCFCOI1 E3 ligase and mediate JA responses. Here, we performed a genetic suppressor screen using the leaky coi1-2 (COI1Leu245Phe ) mutant for restored sensitivity to JA, and identified the intragenic suppressor mutation Leu59Phe, which was in the region connecting the F-box and leucine-rich repeats domains of COI1. The L59F substitution not only restores the COI1L245F function, but also the COI1Gly434Glu (coi1-22rsp ) function in JA responses, through recovering their interactions with ASK1 or ASK2 and their protein levels. The L59F change itself could not enhance the interactions between COI1 and ASK1/2, nor affect JA responses. The present study reveals that the Leu59Phe substitution compensates for the effect of some deleterious mutations in the JA receptor COI1.
Asunto(s)
Proteínas de Arabidopsis/genética , Arabidopsis/genética , Supresión Genética , Sustitución de Aminoácidos , Animales , Antocianinas/metabolismo , Arabidopsis/efectos de los fármacos , Arabidopsis/fisiología , Proteínas de Arabidopsis/metabolismo , Botrytis/patogenicidad , Ciclopentanos/farmacología , Resistencia a la Enfermedad/genética , Flores/genética , Flores/crecimiento & desarrollo , Regulación de la Expresión Génica de las Plantas/efectos de los fármacos , Herbivoria , Oxilipinas/farmacología , Enfermedades de las Plantas/genética , Enfermedades de las Plantas/microbiología , Plantas Modificadas Genéticamente , Proteínas Ligasas SKP Cullina F-box/genética , Proteínas Ligasas SKP Cullina F-box/metabolismo , SpodopteraRESUMEN
The phytohormones ethylene (ET) and jasmonate (JA) regulate plant development, growth, and defense responses; however, the molecular basis for their signaling crosstalk is unclear. Here, we show that JA-ZIM-domain (JAZ) proteins, which repress JA signaling, repress trichome initiation/branching and anthocyanin accumulation, and inhibit the transcriptional activity of the basic helix-loop-helix (bHLH)-MYB members (GLABRA3 (GL3)-GL1 and TRANSPARENT TESTA 8 (TT8)-MYB75) of WD-repeat/bHLH/MYB (WBM) complexes. The ET-stabilized transcription factors ETHYLENE-INSENSITIVE3 (EIN3) and EIN3-LIKE1 (EIL1) were found to bind to several members of WBM complexes, including GL3, ENHANCER OF GLABRA3 (EGL3), TT8, GL1, MYB75, and TRANSPARENT TESTA GLABRA1 (TTG1). This binding repressed the transcriptional activity of the bHLH-MYB proteins and inhibited anthocyanin accumulation, trichome formation, and defenses against insect herbivores while promoting root hair formation. Conversely, the JA-activated bHLH members GL3, EGL3, and TT8 of WBM complexes were able to interact with and attenuate the transcriptional activity of EIN3/EIL1 at the HOOKLESS1 promoter, and their overexpression inhibited apical hook formation. Thus, this study demonstrates a molecular framework for signaling crosstalk between JA and ET in plant development, secondary metabolism, and defense responses.
Asunto(s)
Proteínas de Arabidopsis , Arabidopsis , Animales , Antocianinas/metabolismo , Arabidopsis/metabolismo , Proteínas de Arabidopsis/metabolismo , Factores de Transcripción con Motivo Hélice-Asa-Hélice Básico/genética , Factores de Transcripción con Motivo Hélice-Asa-Hélice Básico/metabolismo , Ciclopentanos , Etilenos/metabolismo , Regulación de la Expresión Génica de las Plantas , Herbivoria , Insectos , Oxilipinas , Tricomas/metabolismoRESUMEN
In response to jasmonates (JAs), the JA receptor Coronatine Insensitive 1 (COI1) recruits JA-zinc-finger inflorescence meristem (ZIM)-domain (JAZ) family repressors for destruction to regulate plant growth, development, and defense. As Arabidopsis encodes 13 JAZ repressors, their functional specificity, diversity, and redundancy in JA/COI1-mediated responses remain unclear. We generated a broad range of jaz mutants based on their phylogenetic relationship to investigate their roles in JA responses. The group I JAZ6 may play an inhibitory role in resistance to Botrytis cinerea, group II (JAZ10)/III (JAZ11/12) in JA-regulated root growth inhibition and susceptibility to Pseudomonas syringae pv tomato DC3000, and group IV JAZ3/4/9 in flowering time delay and defense against insects. JAZs exhibit high redundancy in apical hook curvature. The undecuple jaz1/2/3/4/5/6/7/9/10/11/12 (jaz1-7,9-12) mutations enhance JA responses and suppress the phenotypes of coi1-1 in flowering time, rosette growth, and defense. The JA hypersensitivity of jaz1-7,9-12 in root growth, hook curvature, and leaf yellowing is blocked by coi1-1. jaz1-7,9-12 does not influence the stamen phenotypes of wild-type and coi1-1. jaz1-7,9-12 affects JA-regulated transcriptional profile and recovers a fraction of that in coi1-1. This study contributes to elucidating the specificity, diversity, and redundancy of JAZ members in JA/COI1-regulated growth, development, and defense responses.
Asunto(s)
Proteínas de Arabidopsis , Arabidopsis , Arabidopsis/genética , Arabidopsis/metabolismo , Proteínas de Arabidopsis/genética , Proteínas de Arabidopsis/metabolismo , Botrytis , Ciclopentanos , Regulación de la Expresión Génica de las Plantas , Oxilipinas , Filogenia , Proteínas Represoras/genética , Proteínas Represoras/metabolismoRESUMEN
Effector-triggered immunity (ETI) in plants involves a large family of nucleotide-binding leucine-rich repeat (NLR) immune receptors, including Toll/IL-1 receptor-NLRs (TNLs) and coiled-coil NLRs (CNLs). Although various NLR immune receptors are known, a mechanistic understanding of NLR function in ETI remains unclear. The TNL Recognition of XopQ 1 (Roq1) recognizes the effectors XopQ and HopQ1 from Xanthomonas and Pseudomonas, respectively, which activates resistance to Xanthomonas euvesicatoria and Xanthomonas gardneri in an Enhanced Disease Susceptibility 1 (EDS1)-dependent way in Nicotiana benthamiana In this study, we found that the N. benthamiana N requirement gene 1 (NRG1), a CNL protein required for the tobacco TNL protein N-mediated resistance to tobacco mosaic virus, is also essential for immune signaling [including hypersensitive response (HR)] triggered by the TNLs Roq1 and Recognition of Peronospora parasitica 1 (RPP1), but not by the CNLs Bs2 and Rps2, suggesting that NRG1 may be a conserved key component in TNL signaling pathways. Besides EDS1, Roq1 and NRG1 are necessary for resistance to Xanthomonas and Pseudomonas in N. benthamiana NRG1 functions downstream of Roq1 and EDS1 and physically associates with EDS1 in mediating XopQ-Roq1-triggered immunity. Moreover, RNA sequencing analysis showed that XopQ-triggered gene-expression profile changes in N. benthamiana were almost entirely mediated by Roq1 and EDS1 and were largely regulated by NRG1. Overall, our study demonstrates that NRG1 is a key component that acts downstream of EDS1 to mediate various TNL signaling pathways, including Roq1 and RPP1-mediated HR, resistance to Xanthomonas and Pseudomonas, and XopQ-regulated transcriptional changes in N. benthamiana.
Asunto(s)
Nicotiana/genética , Nicotiana/metabolismo , Subgrupos de Linfocitos B/metabolismo , Proteínas de Unión al ADN , Proteínas Repetidas Ricas en Leucina , Proteínas NLR/metabolismo , Neurregulina-1/genética , Neurregulina-1/fisiología , Enfermedades de las Plantas , Inmunidad de la Planta , Proteínas de Plantas/genética , Dominios Proteicos , Proteínas/genética , Pseudomonas , Transducción de Señal , Transcriptoma , XanthomonasRESUMEN
The immune pathway responsible for perception of the Xanthomonas perforans effector XopJ4 was identified in the plant Nicotiana benthamiana. This pathogen causes significant yield loss in commercial tomato cultivation. Genetic mapping and viral-induced gene silencing were used to identify immune signaling components of the XopJ4 perception pathway in N. benthamiana. Transient complementation assays were performed to determine the functionality of gene variants and co-immunoprecipitation assays were used to gain insight into the molecular mechanism of the pathway. Two N. benthamiana ethyl methanesulfonate (EMS) mutants deficient for XopJ4 perception were identified as having loss-of-function mutations in the gene encoding the nucleotide binding, leucine-rich repeat (NLR) protein NbZAR1. Silencing of a receptor-like cytoplasmic kinase family XII gene, subsequently named XOPJ4 IMMUNITY 2 (JIM2), blocks perception of XopJ4. This study demonstrates the feasibility of conducting mutant screens in N. benthamiana to investigate the genetic basis of the plant immune system and other processes. The identification of NbZAR1 and JIM2 as mediating XopJ4 perception in N. benthamiana supports the model of ZAR1 being involved in the perception of many different pathogen effector proteins with specificity dictated by associated receptor-like cytoplasmic kinases.
Asunto(s)
Proteínas Bacterianas/metabolismo , Nicotiana/genética , Enfermedades de las Plantas/inmunología , Inmunidad de la Planta , Proteínas de Plantas/metabolismo , Transducción de Señal , Xanthomonas/fisiología , Proteínas Bacterianas/genética , Solanum lycopersicum/genética , Solanum lycopersicum/inmunología , Solanum lycopersicum/microbiología , Proteínas NLR/genética , Proteínas NLR/metabolismo , Enfermedades de las Plantas/microbiología , Proteínas de Plantas/genética , Nicotiana/inmunología , Nicotiana/microbiologíaRESUMEN
Xanthomonas spp. are phytopathogenic bacteria that can cause disease on a wide variety of plant species resulting in significant impacts on crop yields. Limited genetic resistance is available in most crop species and current control methods are often inadequate, particularly when environmental conditions favor disease. The plant Nicotiana benthamiana has been shown to be resistant to Xanthomonas and Pseudomonas due to an immune response triggered by the bacterial effector proteins XopQ and HopQ1, respectively. We used a reverse genetic screen to identify Recognition of XopQ 1 (Roq1), a nucleotide-binding leucine-rich repeat (NLR) protein with a Toll-like interleukin-1 receptor (TIR) domain, which mediates XopQ recognition in N. benthamiana. Roq1 orthologs appear to be present only in the Nicotiana genus. Expression of Roq1 was found to be sufficient for XopQ recognition in both the closely-related Nicotiana sylvestris and the distantly-related beet plant (Beta vulgaris). Roq1 was found to co-immunoprecipitate with XopQ, suggesting a physical association between the two proteins. Roq1 is able to recognize XopQ alleles from various Xanthomonas species, as well as HopQ1 from Pseudomonas, demonstrating widespread potential application in protecting crop plants from these pathogens.
Asunto(s)
Resistencia a la Enfermedad , Nicotiana/metabolismo , Enfermedades de las Plantas/microbiología , Proteínas de Plantas/metabolismo , Pseudomonas/metabolismo , Xanthomonas/metabolismo , Proteínas Bacterianas/metabolismoRESUMEN
Stamens are the plant male reproductive organs essential for plant fertility. Proper development of stamens is modulated by environmental cues and endogenous hormone signals. Deficiencies in biosynthesis or perception of the phytohormone jasmonate (JA) attenuate stamen development, disrupt male fertility, and abolish seed production in Arabidopsis thaliana. This study revealed that JA-mediated stamen development and seed production are regulated by a bHLH-MYB complex. The IIIe basic helix-loop-helix (bHLH) transcription factor MYC5 acts as a target of JAZ repressors to function redundantly with other IIIe bHLH factors such as MYC2, MYC3, and MYC4 in the regulation of stamen development and seed production. The myc2 myc3 myc4 myc5 quadruple mutant exhibits obvious defects in stamen development and significant reduction in seed production. Moreover, these IIIe bHLH factors interact with the MYB transcription factors MYB21 and MYB24 to form a bHLH-MYB transcription complex and cooperatively regulate stamen development. We speculate that the JAZ proteins repress the bHLH-MYB complex to suppress stamen development and seed production, while JA induces JAZ degradation and releases the bHLH-MYB complex to subsequently activate the expression of downstream genes essential for stamen development and seed production.
Asunto(s)
Proteínas de Arabidopsis/fisiología , Arabidopsis/crecimiento & desarrollo , Factores de Transcripción con Motivo Hélice-Asa-Hélice Básico/fisiología , Ciclopentanos/metabolismo , Flores/crecimiento & desarrollo , Oxilipinas/metabolismo , Reguladores del Crecimiento de las Plantas/fisiología , Semillas/crecimiento & desarrollo , Factores de Transcripción/fisiología , Arabidopsis/fisiología , Regulación de la Expresión Génica de las Plantas/fisiología , Transactivadores/fisiologíaRESUMEN
Plants initiate leaf senescence to relocate nutrients and energy from aging leaves to developing tissues or storage organs for growth, reproduction, and defense. Leaf senescence, the final stage of leaf development, is regulated by various environmental stresses, developmental cues, and endogenous hormone signals. Jasmonate (JA), a lipid-derived phytohormone essential for plant defense and plant development, serves as an important endogenous signal to activate senescence-associated gene expression and induce leaf senescence. This study revealed one of the mechanisms underlying JA-induced leaf senescence: antagonistic interactions of the bHLH subgroup IIIe factors MYC2, MYC3, and MYC4 with the bHLH subgroup IIId factors bHLH03, bHLH13, bHLH14, and bHLH17. We showed that MYC2, MYC3, and MYC4 function redundantly to activate JA-induced leaf senescence. MYC2 binds to and activates the promoter of its target gene SAG29 (SENESCENCE-ASSOCIATED GENE29) to activate JA-induced leaf senescence. Interestingly, plants have evolved an elaborate feedback regulation mechanism to modulate JA-induced leaf senescence: The bHLH subgroup IIId factors (bHLH03, bHLH13, bHLH14, and bHLH17) bind to the promoter of SAG29 and repress its expression to attenuate MYC2/MYC3/MYC4-activated JA-induced leaf senescence. The antagonistic regulation by activators and repressors would mediate JA-induced leaf senescence at proper level suitable for plant survival in fluctuating environmental conditions.
Asunto(s)
Envejecimiento/fisiología , Arabidopsis/crecimiento & desarrollo , Factores de Transcripción con Motivo Hélice-Asa-Hélice Básico/fisiología , Ciclopentanos/metabolismo , Oxilipinas/metabolismo , Reguladores del Crecimiento de las Plantas/fisiología , Hojas de la Planta/crecimiento & desarrollo , Arabidopsis/fisiología , Proteínas de Arabidopsis/fisiología , Factores de Transcripción Básicos con Cremalleras de Leucinas y Motivos Hélice-Asa-Hélice/fisiología , Regulación de la Expresión Génica de las Plantas/fisiología , Proteínas de la Membrana/fisiología , Hojas de la Planta/fisiología , Regiones Promotoras Genéticas/fisiología , Transactivadores/fisiologíaRESUMEN
Jasmonates (JAs), lipid-derived phytohormones, regulate plant growth, development and defenses against biotic stresses. CORONATINE INSENSITIVE1 perceives bioactive JA and recruits JASMONATE ZIM-DOMAIN (JAZ) proteins for ubiquitination and subsequent degradation via the 26S proteasome, which de-represses JAZ-targeted transcription factors that regulate diverse JA responses. Recent studies showed that the Arabidopsis basic helix-loop-helix transcription factor MYC5 interacts with JAZs and regulates stamen development. However, whether MYC5 mediates other JA responses is unclear. Here, we show that MYC5 functions redundantly with MYC2, MYC3 and MYC4 to modulate JA-regulated root growth inhibition and plant defenses against insect attack and pathogen infection, and that it positively regulates JA-induced leaf senescence. Our findings define MYC5 as an important regulator that is essential for diverse JA responses.
Asunto(s)
Proteínas de Arabidopsis/metabolismo , Arabidopsis/crecimiento & desarrollo , Arabidopsis/inmunología , Factores de Transcripción con Motivo Hélice-Asa-Hélice Básico/metabolismo , Ciclopentanos/farmacología , Oxilipinas/farmacología , Hojas de la Planta/fisiología , Animales , Arabidopsis/genética , Arabidopsis/metabolismo , Proteínas de Arabidopsis/genética , Factores de Transcripción con Motivo Hélice-Asa-Hélice Básico/genética , Botrytis/efectos de los fármacos , Botrytis/fisiología , Resistencia a la Enfermedad/efectos de los fármacos , Regulación de la Expresión Génica de las Plantas/efectos de los fármacos , Herbivoria/efectos de los fármacos , Enfermedades de las Plantas/microbiología , Hojas de la Planta/efectos de los fármacos , Raíces de Plantas/efectos de los fármacos , Raíces de Plantas/crecimiento & desarrollo , Plantas Modificadas Genéticamente , Spodoptera/fisiologíaRESUMEN
Integration of diverse environmental and endogenous signals to coordinately regulate growth, development, and defense is essential for plants to survive in their natural habitat. The hormonal signals gibberellin (GA) and jasmonate (JA) antagonistically and synergistically regulate diverse aspects of plant growth, development, and defense. GA and JA synergistically induce initiation of trichomes, which assist seed dispersal and act as barriers to protect plants against insect attack, pathogen infection, excessive water loss, and UV irradiation. However, the molecular mechanism underlying such synergism between GA and JA signaling remains unclear. In this study, we revealed a mechanism for GA and JA signaling synergy and identified a signaling complex of the GA pathway in regulation of trichome initiation. Molecular, biochemical, and genetic evidence showed that the WD-repeat/bHLH/MYB complex acts as a direct target of DELLAs in the GA pathway and that both DELLAs and JAZs interacted with the WD-repeat/bHLH/MYB complex to mediate synergism between GA and JA signaling in regulating trichome development. GA and JA induce degradation of DELLAs and JASMONATE ZIM-domain proteins to coordinately activate the WD-repeat/bHLH/MYB complex and synergistically and mutually dependently induce trichome initiation. This study provides deep insights into the molecular mechanisms for integration of different hormonal signals to synergistically regulate plant development.
Asunto(s)
Proteínas de Arabidopsis/metabolismo , Factores de Transcripción con Motivo Hélice-Asa-Hélice Básico/metabolismo , Ciclopentanos/metabolismo , Giberelinas/metabolismo , Oxilipinas/metabolismo , Unión Proteica , Transducción de SeñalRESUMEN
Plants have evolved sophisticated mechanisms for integration of endogenous and exogenous signals to adapt to the changing environment. Both the phytohormones jasmonate (JA) and ethylene (ET) regulate plant growth, development, and defense. In addition to synergistic regulation of root hair development and resistance to necrotrophic fungi, JA and ET act antagonistically to regulate gene expression, apical hook curvature, and plant defense against insect attack. However, the molecular mechanism for such antagonism between JA and ET signaling remains unclear. Here, we demonstrate that interaction between the JA-activated transcription factor MYC2 and the ET-stabilized transcription factor ETHYLENE-INSENSITIVE3 (EIN3) modulates JA and ET signaling antagonism in Arabidopsis thaliana. MYC2 interacts with EIN3 to attenuate the transcriptional activity of EIN3 and repress ET-enhanced apical hook curvature. Conversely, EIN3 interacts with and represses MYC2 to inhibit JA-induced expression of wound-responsive genes and herbivory-inducible genes and to attenuate JA-regulated plant defense against generalist herbivores. Coordinated regulation of plant responses in both antagonistic and synergistic manners would help plants adapt to fluctuating environments.
Asunto(s)
Proteínas de Arabidopsis/fisiología , Arabidopsis/metabolismo , Factores de Transcripción Básicos con Cremalleras de Leucinas y Motivos Hélice-Asa-Hélice/fisiología , Ciclopentanos/metabolismo , Etilenos/metabolismo , Proteínas Nucleares/fisiología , Oxilipinas/metabolismo , Transducción de Señal/genética , Factores de Transcripción/fisiología , Arabidopsis/genética , Proteínas de Arabidopsis/genética , Proteínas de Arabidopsis/metabolismo , Factores de Transcripción Básicos con Cremalleras de Leucinas y Motivos Hélice-Asa-Hélice/genética , Factores de Transcripción Básicos con Cremalleras de Leucinas y Motivos Hélice-Asa-Hélice/metabolismo , Proteínas de Unión al ADN , Regulación de la Expresión Génica de las Plantas , Mutación , Proteínas Nucleares/genética , Proteínas Nucleares/metabolismo , Factores de Transcripción/genética , Factores de Transcripción/metabolismoRESUMEN
Plants have evolved sophisticated systems for adaptation to their natural habitat. In response to developmental and environmental cues, plants produce and perceive jasmonate (JA) signals, which induce degradation of JASMONATE-ZIM-Domain (JAZ) proteins and derepress the JAZ-repressed transcription factors to regulate diverse aspects of defense responses and developmental processes. Here, we identified the bHLH subgroup IIId transcription factors (bHLH3, bHLH13, bHLH14 and bHLH17) as novel targets of JAZs. These bHLH subgroup IIId transcription factors act as transcription repressors and function redundantly to negatively regulate JA responses. The quadruple mutant bhlh3 bhlh13 bhlh14 bhlh17 showed severe sensitivity to JA-inhibited root growth and JA-induced anthocyanin accumulation, and exhibited obvious increase in JA-regulated plant defense against pathogen infection and insect attack. Transgenic plants overexpressing bHLH13 or bHLH17 displayed reduced JA responses. Furthermore, these bHLH factors functioned as transcription repressors to antagonize the transcription activators, such as MYC2 and the WD-repeat/bHLH/MYB complex, through binding to their target sequences. Coordinated regulation of JA responses by transcription activators and repressors would benefit plants by allowing fine regulation of defense and development, and survival in their frequently changing environment.
Asunto(s)
Proteínas de Arabidopsis/genética , Arabidopsis/crecimiento & desarrollo , Factores de Transcripción con Motivo Hélice-Asa-Hélice Básico/genética , Ciclopentanos/metabolismo , Oxilipinas/metabolismo , Proteínas Represoras/genética , Antocianinas/metabolismo , Arabidopsis/genética , Arabidopsis/inmunología , Proteínas de Arabidopsis/metabolismo , Factores de Transcripción Básicos con Cremalleras de Leucinas y Motivos Hélice-Asa-Hélice/metabolismo , Regulación de la Expresión Génica de las Plantas , Enfermedades de las Plantas/genética , Enfermedades de las Plantas/inmunología , Plantas Modificadas Genéticamente/genética , Proteínas Represoras/metabolismo , Activación Transcripcional/genética , Técnicas del Sistema de Dos HíbridosRESUMEN
Jasmonates (JAs) mediate plant responses to insect attack, wounding, pathogen infection, stress, and UV damage and regulate plant fertility, anthocyanin accumulation, trichome formation, and many other plant developmental processes. Arabidopsis thaliana Jasmonate ZIM-domain (JAZ) proteins, substrates of the CORONATINE INSENSITIVE1 (COI1)-based SCF(COI1) complex, negatively regulate these plant responses. Little is known about the molecular mechanism for JA regulation of anthocyanin accumulation and trichome initiation. In this study, we revealed that JAZ proteins interact with bHLH (Transparent Testa8, Glabra3 [GL3], and Enhancer of Glabra3 [EGL3]) and R2R3 MYB transcription factors (MYB75 and Glabra1), essential components of WD-repeat/bHLH/MYB transcriptional complexes, to repress JA-regulated anthocyanin accumulation and trichome initiation. Genetic and physiological evidence showed that JA regulates WD-repeat/bHLH/MYB complex-mediated anthocyanin accumulation and trichome initiation in a COI1-dependent manner. Overexpression of the MYB transcription factor MYB75 and bHLH factors (GL3 and EGL3) restored anthocyanin accumulation and trichome initiation in the coi1 mutant, respectively. We speculate that the JA-induced degradation of JAZ proteins abolishes the interactions of JAZ proteins with bHLH and MYB factors, allowing the transcriptional function of WD-repeat/bHLH/MYB complexes, which subsequently activate respective downstream signal cascades to modulate anthocyanin accumulation and trichome initiation.
Asunto(s)
Antocianinas/metabolismo , Proteínas de Arabidopsis/metabolismo , Arabidopsis/metabolismo , Ciclopentanos/metabolismo , Oxilipinas/metabolismo , Transducción de Señal/fisiología , Secuencias de Aminoácidos , Arabidopsis/genética , Proteínas de Arabidopsis/genética , Factores de Transcripción con Motivo Hélice-Asa-Hélice Básico/genética , Factores de Transcripción con Motivo Hélice-Asa-Hélice Básico/metabolismo , Proteínas de Unión al ADN/genética , Proteínas de Unión al ADN/metabolismo , Regulación de la Expresión Génica de las Plantas , Proteínas Nucleares/genética , Proteínas Nucleares/metabolismo , Fenotipo , Reguladores del Crecimiento de las Plantas/metabolismo , Plantas Modificadas Genéticamente/genética , Plantas Modificadas Genéticamente/metabolismo , Estructura Terciaria de Proteína , Proteínas Represoras/genética , Proteínas Represoras/metabolismo , Factores de Transcripción/genética , Factores de Transcripción/metabolismo , Transcripción GenéticaRESUMEN
The Arabidopsis thaliana F-box protein CORONATINE INSENSITIVE1 (COI1) perceives jasmonate (JA) signals and subsequently targets the Jasmonate-ZIM domain proteins (JAZs) for degradation by the SCF(COI1)-26S proteasome pathway to mediate various jasmonate-regulated processes, including fertility, root growth, anthocyanin accumulation, senescence, and defense. In this study, we screened JAZ-interacting proteins from an Arabidopsis cDNA library in the yeast two-hybrid system. MYB21 and MYB24, two R2R3-MYB transcription factors, were found to interact with JAZ1, JAZ8, and JAZ11 in yeast and in planta. Genetic and physiological experiments showed that the myb21 myb24 double mutant exhibited defects specifically in pollen maturation, anther dehiscence, and filament elongation leading to male sterility. Transgenic expression of MYB21 in the coi1-1 mutant was able to rescue male fertility partially but unable to recover JA-regulated root growth inhibition, anthocyanin accumulation, and plant defense. These results demonstrate that the R2R3-MYB transcription factors MYB21 and MYB24 function as direct targets of JAZs to regulate male fertility specifically. We speculate that JAZs interact with MYB21 and MYB24 to attenuate their transcriptional function; upon perception of JA signal, COI1 recruits JAZs to the SCF(COI1) complex for ubiquitination and degradation through the 26S proteasome; MYB21 and MYB24 are then released to activate expression of various genes essential for JA-regulated anther development and filament elongation.
Asunto(s)
Proteínas de Arabidopsis/genética , Arabidopsis/crecimiento & desarrollo , Ciclopentanos/metabolismo , Flores/crecimiento & desarrollo , Oxilipinas/metabolismo , Factores de Transcripción/genética , Antocianinas/análisis , Arabidopsis/genética , Proteínas de Arabidopsis/metabolismo , Clonación Molecular , Flores/metabolismo , Regulación de la Expresión Génica de las Plantas , Datos de Secuencia Molecular , Proteínas Nucleares/metabolismo , Infertilidad Vegetal , Raíces de Plantas/metabolismo , Plantas Modificadas Genéticamente/genética , Plantas Modificadas Genéticamente/crecimiento & desarrollo , Complejo de la Endopetidasa Proteasomal/genética , Proteínas Recombinantes de Fusión/metabolismo , Proteínas Represoras/metabolismo , Plantones/genética , Plantones/crecimiento & desarrollo , Semillas/crecimiento & desarrollo , Nicotiana/genética , Nicotiana/crecimiento & desarrollo , Factores de Transcripción/metabolismoRESUMEN
Polygalacturonase-inhibiting proteins (PGIPs) interact with pathogen-derived polygalacturonases to inhibit their virulence-associated plant cell wall-degrading activity but stimulate immunity-inducing oligogalacturonide production. Here we show that interaction between Phaseolus vulgaris PGIP2 (PvPGIP2) and Fusarium phyllophilum polygalacturonase (FpPG) enhances substrate binding, resulting in inhibition of the enzyme activity of FpPG. This interaction promotes FpPG-catalyzed production of long-chain immunoactive oligogalacturonides, while diminishing immunosuppressive short oligogalacturonides. PvPGIP2 binding creates a substrate binding site on PvPGIP2-FpPG, forming a new polygalacturonase with boosted substrate binding activity and altered substrate preference. Structure-based engineering converts a putative PGIP that initially lacks FpPG-binding activity into an effective FpPG-interacting protein. These findings unveil a mechanism for plants to transform pathogen virulence activity into a defense trigger and provide proof of principle for engineering PGIPs with broader specificity.
Asunto(s)
Fusarium , Phaseolus , Inmunidad de la Planta , Proteínas de Plantas , Poligalacturonasa , Factores de Virulencia , Inmunidad Innata , Proteínas de Plantas/metabolismo , Poligalacturonasa/metabolismo , Factores de Virulencia/metabolismo , Fusarium/inmunología , Fusarium/patogenicidad , Phaseolus/inmunología , Phaseolus/microbiologíaRESUMEN
Plants and animals detect pathogen infection using intracellular nucleotide-binding leucine-rich repeat receptors (NLRs) that directly or indirectly recognize pathogen effectors and activate an immune response. How effector sensing triggers NLR activation remains poorly understood. Here we describe the 3.8-angstrom-resolution cryo-electron microscopy structure of the activated ROQ1 (recognition of XopQ 1), an NLR native to Nicotiana benthamiana with a Toll-like interleukin-1 receptor (TIR) domain bound to the Xanthomonas euvesicatoria effector XopQ (Xanthomonas outer protein Q). ROQ1 directly binds to both the predicted active site and surface residues of XopQ while forming a tetrameric resistosome that brings together the TIR domains for downstream immune signaling. Our results suggest a mechanism for the direct recognition of effectors by NLRs leading to the oligomerization-dependent activation of a plant resistosome and signaling by the TIR domain.