Plant-biotic interaction

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    Trehalose phosphate synthase 5-dependent trehalose metabolism modulates basal defense responses in Arabidopsis thaliana
    Xuelan Wang, Yan Du and Diqiu Yu
    J Integr Plant Biol 2019, 61 (4): 509-527.  
    doi: 10.1111/jipb.12704
    Abstract (Browse 706)  |   Save

    Despite the recent discovery that trehalose synthesis is important for plant development and abiotic stress tolerance, the effects of trehalose on biotic stress responses remain relatively unknown. In this study, we demonstrate that TREHALOSE PHOSPHATE SYNTHASE 5 (TPS5)-dependent trehalose metabolism regulates Arabidopsis thaliana defenses against pathogens (necrotrophic Botrytis cinerea and biotrophic Pseudomonas syringae). Pathogen infection increased trehalose levels and upregulated TPS5 expression. Application of exogenous trehalose significantly improved plant defenses against B. cinerea, but increased the susceptibility of plants to P. syringae. We demonstrate that elevated trehalose biosynthesis, in transgenic plants over-expressing TPS5, also increased the susceptibility to P. syringae, but decreased the disease symptoms caused by B. cinerea. The knockout of TPS5 prevented the accumulation of trehalose and enhanced defense responses against P. syringae. Additionally, we observed that a TPS5-interacting protein (multiprotein bridging factor 1c) was required for induced expression of TPS5 during pathogen infections. Furthermore, we show that trehalose promotes P. syringae growth and disease development, via a mechanism involving suppression of the plant defense gene, Pathogenesis-Related Protein 1. These findings provide insight into the function of TPS5-dependent trehalose metabolism in plant basal defense responses.

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    A change of leadership at JIPB: A message to the plant sciences community
    Chun-Ming Liu and William (Bill) Lucas
    J Integr Plant Biol 2019, 61 (1): 2-3.  
    doi: 10.1111/jipb.12773
    Abstract (Browse 209)  |   Save
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    A common metabolomic signature is observed upon inoculation of rice roots with various rhizobacteria
    Marine Valette, Marjolaine Rey, Florence Gerin, Gilles Comte and Florence WisniewskiDyé
    J Integr Plant Biol 2020, 62 (2): 228-246.  
    DOI: 10.1111/jipb.12810
    Abstract (Browse 210)  |   Save
    Plant growth‐promoting rhizobacteria (PGPR), whose growth is stimulated by root exudates, are able to improve plant growth and health. Among those, bacteria of the genus Azospirillum were shown to affect root secondary metabolite content in rice and maize, sometimes without visible effects on root architecture. Transcriptomic studies also revealed that expression of several genes involved in stress and plant defense was affected, albeit with fewer genes when a strain was inoculated onto its original host cultivar. Here, we investigated, via a metabolic profiling approach, whether rice roots responded differently and with gradual intensity to various PGPR, isolated from rice or not. A common metabolomic signature of nine compounds was highlighted, with the reduced accumulation of three alkylresorcinols and increased accumulation of two hydroxycinnamic acid amides (HCAA), identified as Np‐coumaroylputrescine and N‐feruloylputrescine. This was accompanied by the increased transcription of two genes involved in the N‐feruloylputrescine biosynthetic pathway. Interestingly, exposure to a rice bacterial pathogen triggered a reduced accumulation of these HCAA in roots, a result contrasting with previous reports of increased HCAA content in leaves upon pathogen infection. Accumulation of HCAA, that are potential antimicrobial compounds, might be considered as a primary reaction of plant to bacterial perception.
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    Mechanism of plant immune activation and signaling: Insight from the first solved plant resistosome structure
    Baomin Feng and Dingzhong Tang
    J Integr Plant Biol 2019, 61 (8): 902-907.  
    doi: 10.1111/jipb.12814
    Abstract (Browse 296)  |   Save
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    Osa‐miR167d facilitates infection of Magnaporthe oryzae in rice
    Zhi-Xue Zhao, Qin Feng, Xiao-Long Cao, Yong Zhu, He Wang, Viswanathan Chandran, Jing Fan, Ji-Qun Zhao, Mei Pu, Yan Li and Wen-Ming Wang
    J Integr Plant Biol 2020, 62 (5): 702-715.  
    doi: 10.1111/jipb.12816
    Abstract (Browse 456)  |   Save

    MicroRNAs (miRNAs) play important roles in rice response to Magnaporthe oryzae, the causative agent of rice blast disease. Studying the roles of rice miRNAs is of great significance for the disease control. Osa‐miR167d belongs to a conserved miRNA family targeting auxin responsive factor (ARF) genes that act in developmental and stress‐induced responses. Here, we show that Osa‐miR167d plays a negative role in rice immunity against M. oryzae by suppressing its target gene. The expression of Osa‐miR167d was significantly suppressed in a resistant accession at and after 24 h post inoculation (hpi), however, its expression was significantly increased at 24 hpi in the susceptible accession upon M. oryzae infection. Transgenic rice lines over‐expressing Osa‐miR167d were highly susceptible to multiple blast fungal strains. By contrast, transgenic lines expressing a target mimicry to block Osa‐miR167d enhanced resistance to rice blast disease. In addition, knocking out the target gene ARF12 led to hyper‐susceptibility to multiple blast fungal strains. Taken together, our results indicate that Osa‐miR167d negatively regulate rice immunity to facilitate the infection of M. oryzae by downregulating ARF12. Thus, Osa‐miR167d‐ARF12 regulatory module could be valuable in improvement of blast‐disease resistance.

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    MdWRKY15 improves resistance of apple to Botryosphaeria dothidea via the salicylic acid-mediated pathway by directly binding the MdICS1 promoter
    Xian-Yan Zhao, Chen-Hui Qi, Han Jiang, Ming-Shuang Zhong, Chun-Xiang You, Yuan-Yuan Li and Yu-Jin Hao
    J Integr Plant Biol 2020, 62 (4): 527-543.  
    doi: 10.1111/jipb.12825
    Abstract (Browse 494)  |   Save

    Isochorismate synthase (ICS) plays an essential role in the accumulation of salicylic acid (SA) and plant disease resistance. Diseases caused by Botryosphaeria dothidea affect apple yields. Thus, it is important to understand the role of ICS1 in disease resistance to B. dothidea in apple. In this study, SA treatment enhanced the resistance to B. dothidea. MdICS1 was induced by B. dothidea and enhanced the resistance to B. dothidea. MdICS1 promoter analysis indicated that the W‐box was vital for the response to B. dothidea treatment. MdWRKY15 was found to interact with the W‐box using yeast one‐hybrid screening. Subsequently, the interaction was confirmed by EMSA, yeast one‐hybrid, ChIP‐PCR, and quantitative PCR assays. Moreover, luciferase and GUS analysis further indicated that MdICS1 was transcriptionally activated by MdWRKY15. Finally, we found the function of MdWRKY15 in the resistance to B. dothidea was partially dependent on MdICS1 from the phenotype of transgenic apples and calli. In summary, we revealed that MdWRKY15 activated the transcription of MdICS1 by directly binding to its promoter to increase the accumulation of SA and the expression of disease‐related genes, thereby resulting in the enhanced resistance to B. dothidea in the SA biosynthesis pathway.

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    Type one protein phosphatases (TOPPs) contribute to the plant defense response in Arabidopsis
    Yaqiong Liu, Jia Yan, Qianqian Qin, Jing Zhang, Yan Chen, Lulu Zhao, Kai He and Suiwen Hou
    J Integr Plant Biol 2020, 62 (3): 360-377.  
    DOI: 10.1111/jipb.12845
    Abstract (Browse 358)  |   Save

    Plant immunity must be tightly controlled to avoid activation of defense mechanisms in the absence of pathogen attack. Protein phosphorylation is a common mechanism regulating immune signaling. In Arabidopsis thaliana, nine members of the type one protein phosphatase (TOPP) family (also known as protein phosphatase 1, PP1) have been identified. Here, we characterized the autoimmune phenotype of topp4‐1, a previously identified dominant‐negative mutant of TOPP4. Epistasis analysis showed that defense activation in topp4‐1 depended on NON‐RACE‐SPECIFIC DISEASE RESISTANCE1, PHYTOALEXIN DEFICIENT4, and the salicylic acid pathway. We generated topp1/4/5/6/7/8/9 septuple mutants to investigate the function of TOPPs in plant immunity. Elevated defense gene expression and enhanced resistance to Pseudomonas syringae pv. tomato (Pst) DC3000 in the septuple mutant indicate that TOPPs function in plant defense responses. Furthermore, TOPPs physically interacted with mitogen‐activated protein kinases (MAPKs) and affected the MAPK‐mediated downstream defense pathway. Thus, our study reveals that TOPPs are important regulators of plant immunity.

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    Identification of plant genes putatively involved in the perception of fungal ergosterol-squalene
    Laura Lindo, Rosa E. Cardoza, Alicia Lorenzana, Pedro A. Casquero and Santiago Gutiérrez
    J Integr Plant Biol 2020, 62 (7): 927-947.  
    doi: 10.1111/jipb.12862
    Abstract (Browse 225)  |   Save

    Trichoderma biocontrol strains establish a complex network of interactions with plants, in which diverse fungal molecules are involved in the recognition of these fungi as nonpathogenic organisms. These molecules act as microbial‐associated molecular patterns that trigger plant responses. Previous studies have reported the importance of ergosterol produced by Trichoderma spp. for the ability of these fungi to induce plant growth and defenses. In addition, squalene, a sterol biosynthetic intermediate, seems to play an important role in these interactions. Here, we analyzed the effect of different concentrations of ergosterol and squalene on tomato (Solanum lycopersicum ) growth and on the transcription level of defense‐ and growth‐related genes. We used an RNA‐seq strategy to identify several tomato genes encoding predicted pattern recognition receptor proteins or WRKY transcription factors, both of which are putatively involved in the perception and response to ergosterol and squalene. Finally, an analysis of Arabidopsis thaliana mutants lacking the genes homologous to these tomato candidates led to the identification of a WRKY40 transcription factor that negatively regulates salicylic acid‐related genes and positively regulates ethylene‐ and jasmonate‐related genes in the presence of ergosterol and squalene.

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    Editing of an effector gene promoter sequence impacts plant‐Phytophthora interaction
    Sylvans Ochola, Jie Huang, Haider Ali, Haidong Shu, Danyu Shen, Min Qiu, Liyuan Wang, Xi Li, Han Chen, Alex Kange, Dinah Qutob and Suomeng Dong
    J Integr Plant Biol 2020, 62 (3): 378-392.  
    DOI: 10.1111/jipb.12883
    Abstract (Browse 354)  |   Save

    Pathogen avirulence (Avr) effectors interplay with corresponding plant resistance (R) proteins and activate robust plant immune responses. Although the expression pattern of Avr genes has been tied to their functions for a long time, it is still not clear how Avr gene expression patterns impact plant‐microbe interactions. Here, we selected PsAvr3b, which shows a typical effector gene expression pattern from a soybean root pathogen Phytophthora sojae. To modulate gene expression, we engineered PsAvr3b promoter sequences by in situ substitution with promoter sequences from Actin (constitutive expression), PsXEG1 (early expression), and PsNLP1 (later expression) using the CRISPR/Cas9. PsAvr3b driven by different promoters resulted in distinct expression levels across all the tested infection time points. Importantly, those mutants with low PsAvr3b expression successfully colonized soybean plants carrying the cognate R gene Rps3b. To dissect the difference in plant responses to the PsAvr3b expression level, we conducted RNA‐sequencing of different infection samples at 24 h postinfection and found soybean immune genes, including a few previously unknown genes that are associated with resistance. Our study highlights that fine‐tuning in Avr gene expression impacts the compatibility of plant disease and provides clues to improve crop resistance in disease control management.

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    Plant immune signaling: Advancing on two frontiers
    Wei Wang, Baomin Feng, Jian-Min Zhou and Dingzhong Tang
    J Integr Plant Biol 2020, 62 (1): 2-24.  
    doi: 10.1111/jipb.12898
    Abstract (Browse 806)  |   Save

    Plants have evolved multiple defense strategies to cope with pathogens, among which plant immune signaling that relies on cell‐surface localized and intracellular receptors takes fundamental roles. Exciting breakthroughs were made recently on the signaling mechanisms of pattern recognition receptors (PRRs) and intracellular nucleotide‐binding site (NBS) and leucine‐rich repeat (LRR) domain receptors (NLRs). This review summarizes the current view of PRRs activation, emphasizing the most recent discoveries about PRRs’ dynamic regulation and signaling mechanisms directly leading to downstream molecular events including mitogen‐activated protein kinase (MAPK) activation and calcium (Ca2+) burst. Plants also have evolved intracellular NLRs to perceive the presence of specific pathogen effectors and trigger more robust immune responses. We also discuss the current understanding of the mechanisms of NLR activation, which has been greatly advanced by recent breakthroughs including structures of the first full‐length plant NLR complex, findings of NLR sensor‐helper pairs and novel biochemical activity of Toll/interleukin‐1 receptor (TIR) domain.

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    MYC2, MYC3, and MYC4 function additively in wounding-induced jasmonic acid biosynthesis and catabolism
    Cuiping Zhang, Yunting Lei, Chengkai Lu, Lei Wang and Jianqiang Wu
    J Integr Plant Biol 2020, 62 (8): 1159-1175.  
    DOI: 10.1111/jipb.12902
    Abstract (Browse 474)  |   Save

    Jasmonic acid (JA) plays a critical role in plant defenses against insects and necrotrophic fungi. Wounding or lepidopteran insect feeding rapidly induces a burst of JA in plants, which usually reaches peak values within 1 to 2 h. The induced JA is converted to JA‐Ile and perceived by the COI1‐JAZ co‐receptor, leading to activation of the transcription factors MYC2 and its homologs, which further induce JA‐responsive genes. Although much is known about JA biosynthesis and catabolism enzymes and JA signaling, how JA biosynthesis and catabolism are regulated remain unclear. Here, we show that in Arabidopsis thaliana MYC2 functions additively with MYC3 and MYC4 to regulate wounding‐induced JA accumulation by directly binding to the promoters of genes function in JA biosynthesis and catabolism to promote their transcription. MYC2 also controls the transcription of JAV1 and JAM1 , which are key factors controlling JA biosynthesis and catabolism, respectively. In addition, we also found that MYC2 could bind to the MYC2 promoter and self‐inhibit its own expression. This work illustrates the central role of MYC2/3/4 in controlling wounding‐induced JA accumulation by regulating the transcription of genes involved in JA biosynthesis and catabolism.

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    Co-regulation of indole glucosinolates and camalexin biosynthesis by CPK5/CPK6 and MPK3/MPK6 signaling pathways
    Liuyi Yang, Yan Zhang, Rongxia Guan, Sen Li, Xuwen Xu, Shuqun Zhang and Juan Xu
    J Integr Plant Biol 2020, 62 (11): 1780-1796.  
    doi: 10.1111/jipb.12973
    Abstract (Browse 587)  |   Save

    Secondary plant metabolites, represented by indole glucosinolates (IGS) and camalexin, play important roles in Arabidopsis immunity. Previously, we demonstrated the importance of MPK3 and MPK6, two closely related MAPKs, in regulating Botrytis cinerea (Bc)‐induced IGS and camalexin biosynthesis. Here we report that CPK5 and CPK6, two redundant calcium‐dependent protein kinases (CPKs), are also involved in regulating the biosynthesis of these secondary metabolites. The loss‐of‐function of both CPK5 and CPK6 compromises plant resistance to Bc. Expression profiling of CPK5‐VK transgenic plants, in which a truncated constitutively active CPK5 is driven by a steroid‐inducible promoter, revealed that biosynthetic genes of both IGS and camalexin pathways are coordinately upregulated after the induction of CPK5‐VK, leading to high‐level accumulation of camalexin and 4‐methoxyindole‐3‐yl‐methylglucosinolate (4MI3G). Induction of camalexin and 4MI3G, as well as the genes in their biosynthesis pathways, is greatly compromised in cpk5 cpk6 mutant in response to Bc. In a conditional cpk5 cpk6 mpk3 mpk6 quadruple mutant, Bc resistance and induction of IGS and camalexin are further reduced in comparison to either cpk5 cpk6 or conditional mpk3 mpk6 double mutant, suggesting that both CPK5/CPK6 and MPK3/MPK6 signaling pathways contribute to promote the biosynthesis of 4MI3G and camalexin in defense against Bc.

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    Receptor‐like kinases MDS1 and MDS2 promote SUMM2‐mediated immunity
    Yanan Liu, Xionghui Zhong, Zhibin Zhang, Jiameng Lan, Xingchuan Huang, Hainan Tian, Xin Li and Yuelin Zhang
    J Integr Plant Biol 2021, 63 (2): 277-282.  
    doi: 10.1111/jipb.12978
    Abstract (Browse 549)  |   Save
    Disruption of the MEKK1‐MKK1/MKK2‐MPK4 kinase cascade leads to activation of immunity mediated by the nucleotide‐binding leucine‐rich repeat (NLR) immune receptor SUMM2, which monitors the phosphorylation status of CRCK3. Here we report that two receptor‐like kinases (RLKs), MDS1, and MDS2, function redundantly to promote SUMM2‐mediated immunity. Activation of SUMM2‐mediated immunity is dependent on MDS1, and to a less extent on MDS2. MDS1 associates with CRCK3 in planta and can phosphorylate CRCK3 in vitro, suggesting that it may target CRCK3 to positively regulate SUMM2‐mediated signaling. Our finding highlights a new defense mechanism where RLKs promote NLR‐mediated immunity.
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    Deficiency of mitochondrial outer membrane protein 64 confers rice resistance to both piercing‐sucking and chewing insects in rice
    Hui‐Min Guo, Hai‐Chao Li, Shi‐Rong Zhou, Hong‐Wei Xue and Xue‐Xia Miao
    J Integr Plant Biol 2020, 62 (12): 1967-1982.  
    DOI: 10.1111/jipb.12983
    Abstract (Browse 296)  |   Save

    The brown planthopper (BPH) and striped stem borer (SSB) are the most devastating insect pests in rice (Oryza sativa ) producing areas. Screening for endogenous resistant genes is the most practical strategy for rice insect‐resistance breeding. Forty‐five mutants showing high resistance against BPH were identified in a rice T‐DNA insertion population (11,000 putative homozygous lines) after 4 years of large‐scale field BPH‐resistance phenotype screening. Detailed analysis showed that deficiency of rice mitochondrial outer membrane protein 64 (OM64 ) gene resulted in increased resistance to BPH. Mitochondrial outer membrane protein 64 protein is located in the outer mitochondrial membrane by subcellular localization and its deficiency constitutively activated hydrogen peroxide (H2O2) signaling, which stimulated antibiosis and tolerance to BPH. The om64 mutant also showed enhanced resistance to SSB, a chewing insect, which was due to promotion of Jasmonic acid biosynthesis and related responses. Importantly, om64 plants presented no significant changes in rice yield‐related characters. This study confirmed OM64 as a negative regulator of rice herbivore resistance through regulating H2O2 production. Mitochondrial outer membrane protein 64 is a potentially efficient candidate to improve BPH and SSB resistance through gene deletion. Why the om64 mutant was resistant to both piercing‐sucking and chewing insects via a gene deficiency in mitochondria is discussed.

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    Fg12 ribonuclease secretion contributes to Fusarium graminearum virulence and induces plant cell death
    Bo Yang, Yuyin Wang, Mengjun Tian, Kaixin Dai, Wenyue Zheng, Zehan Liu, Sen Yang, Xinyu Liu, Dongya Shi, Haifeng Zhang, Yan Wang, Wenwu Ye and Yuanchao Wang
    J Integr Plant Biol 2021, 63 (2): 365-377.  
    doi: 10.1111/jipb.12997
    Abstract (Browse 470)  |   Save
    Filamentous fungal pathogens secrete effectors that modulate host immunity and facilitate infection. Fusarium graminearum is an important plant pathogen responsible for various devastating diseases. However, little is known about the function of effector proteins secreted by F. graminearum. Herein, we identified several effector candidates in the F. graminearum secretome. Among them, the secreted ribonuclease Fg12 was highly upregulated during the early stages of F. graminearum infection in soybean; its deletion compromised the virulence of F. graminearum. Transient expression of Fg12 in Nicotiana benthamiana induced cell death in a light‐dependent manner. Fg12 possessed ribonuclease (RNase) activity, degrading total RNA. The enzymatic activity of Fg12 was required for its cell death‐promoting effects. Importantly, the ability of Fg12 to induce cell death was independent of BAK1/SOBIR1, and treatment of soybean with recombinant Fg12 protein induced resistance to various pathogens, including F. graminearum and Phytophthora sojae. Overall, our results provide evidence that RNase effectors not only contribute to pathogen virulence but also induce plant cell death.
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    Arabidopsis E3 ligase KEG associates with and ubiquitinates MKK4 and MKK5 to regulate plant immunity
    Chenyang Gao, Pengwei Sun, Wei Wang and Dingzhong Tang
    J Integr Plant Biol 2021, 63 (2): 327-339.  
    doi: 10.1111/jipb.13007
    Abstract (Browse 712)  |   Save
    Mitogen‐activated protein kinase (MAPK) cascades are highly conserved signaling modules that regulate plant immune responses. The Arabidopsis thaliana Raf‐like MAPK kinase kinase ENHANCED DISEASE RESISTANCE1 (EDR1) is a key negative regulator of plant immunity that affects the protein levels of MKK4 and MKK5, two important MAPK cascade members, but the underlying mechanism is poorly understood. Here, genome‐wide phosphorylation analysis demonstrated that the E3 ligase KEEP ON GOING (KEG) is phosphorylated in the edr1 mutant but not the wild type, suggesting that EDR1 negatively affects KEG phosphorylation. The identified phosphorylation sites in KEG appear to be important for its accumulation. The keg‐4 mutant, a previously identified edr1 suppressor, enhances susceptibility to the powdery mildew pathogen Golovinomyces cichoracearum. In addition, MKK4 and MKK5 protein levels are reduced in the keg‐4 mutant. Furthermore, we demonstrate that MKK4 and MKK5 associate with full‐length KEG, but not with truncated KEG‐RK or KEG‐RKA, and that KEG ubiquitinates and mediates the degradation of MKK4 and MKK5. Taken together, these results indicate that MKK4 and MKK5 protein levels are regulated by KEG via ubiquitination, uncovering a mechanism by which plants fine‐tune immune responses by regulating the homeostasis of key MAPK cascade members via ubiquitination and degradation.
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    ANNEXIN 8 negatively regulates RPW8.1‐mediated cell death and disease resistance in Arabidopsis
    Zhi‐Xue Zhao, Yong‐Ju Xu, Yang Lei, Qin Li, Ji‐Qun Zhao, Yan Li, Jing Fan, Shunyuan Xiao and Wen‐Ming Wang
    J Integr Plant Biol 2021, 63 (2): 378-392.  
    doi: 10.1111/jipb.13025
    Abstract (Browse 371)  |   Save
    Study on the regulation of broad‐spectrum resistance is an active area in plant biology. RESISTANCE TO POWDERY MILDEW 8.1 (RPW8.1) is one of a few broad‐spectrum resistance genes triggering the hypersensitive response (HR) to restrict multiple pathogenic infections. To address the question how RPW8.1 signaling is regulated, we performed a genetic screen and tried to identify mutations enhancing RPW8.1‐mediated HR. Here, we provided evidence to connect an annexin protein with RPW8.1‐mediated resistance in Arabidopsis against powdery mildew. We isolated and characterized Arabidopsis b7‐6 mutant. A point mutation in b7‐6 at the At5g12380 locus resulted in an amino acid substitution in ANNEXIN 8 (AtANN8). Loss‐of‐function or RNA‐silencing of AtANN8 led to enhanced expression of RPW8.1, RPW8.1‐dependent necrotic lesions in leaves, and defense against powdery mildew. Conversely, over‐expression of AtANN8 compromised RPW8.1‐mediated disease resistance and cell death. Interestingly, the mutation in AtANN8 enhanced RPW8.1‐triggered H2O2. In addition, mutation in AtANN8 led to hypersensitivity to salt stress. Together, our data indicate that AtANN8 is involved in multiple stress signaling pathways and negatively regulates RPW8.1‐mediated resistance against powdery mildew and cell death, thus linking ANNEXIN's function with plant immunity.
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    Three‐dimensional reconstruction and comparison of vacuolar membranes in response to viral infection
    Xueting Wang, Juncai Ma, Xuejiao Jin, Ning Yue, Peng Gao, Keith Ka Ki Mai, Xian‐Bing Wang, Dawei Li, Byung‐Ho Kang and Yongliang Zhang
    J Integr Plant Biol 2021, 63 (2): 353-364.  
    doi: 10.1111/jipb.13027
    Abstract (Browse 295)  |   Save
    The vacuole is a unique plant organelle that plays an important role in maintaining cellular homeostasis under various environmental stress conditions. However, the effects of biotic stress on vacuole structure has not been examined using three‐dimensional (3D) visualization. Here, we performed 3D electron tomography to compare the ultrastructural changes in the vacuole during infection with different viruses. The 3D models revealed that vacuoles are remodeled in cells infected with cucumber mosaic virus (CMV) or tobacco necrosis virus A Chinese isolate (TNV‐AC), resulting in the formation of spherules at the periphery of the vacuole. These spherules contain neck‐like channels that connect their interior with the cytosol. Confocal microscopy of CMV replication proteins 1a and 2a and TNV‐AC auxiliary replication protein p23 showed that all of these proteins localize to the tonoplast. Electron microscopy revealed that the expression of these replication proteins alone is sufficient to induce spherule formation on the tonoplast, suggesting that these proteins play prominent roles in inducing vacuolar membrane remodeling. This is the first report of the 3D structures of viral replication factories built on the tonoplasts. These findings contribute to our understanding of vacuole biogenesis under normal conditions and during assembly of plant (+) RNA virus replication complexes.
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    Pathogen‐informed breeding for crop disease resistance
    Qi Li, Bi Wang, Jinping Yu and Daolong Dou
    J Integr Plant Biol 2021, 63 (2): 305-311.  
    doi: 10.1111/jipb.13029
    Abstract (Browse 292)  |   Save
    The development of durable and broad‐spectrum resistance is an economical and eco‐friendly approach to control crop diseases for sustainable agricultural production. Emerging knowledge of the molecular basis of pathogenesis and plant–pathogen interactions has contributed to the development of novel pathogen‐informed breeding strategies beyond the limits imposed by conventional breeding. Here, we review the current status of pathogen‐assisted resistance‐related gene cloning. We also describe how pathogen effector proteins can be used to identify resistance resources and to inform cultivar deployment. Finally, we summarize the main approaches for pathogen‐directed plant improvement, including transgenesis and genome editing. Thus, we describe the emerging role of pathogen‐related studies in the breeding of disease‐resistant varieties, and propose innovative pathogen‐informed strategies for future applications.
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    Nicotiana benthamiana LRR‐RLP NbEIX2 mediates the perception of an EIX‐like protein from Verticillium dahliae
    Zhiyuan Yin, Nan Wang, Lei Pi, Lei Li, Weiwei Duan, Xiaodan Wang and Daolong Dou
    J Integr Plant Biol 2021, 63 (5): 949-960.  
    DOI: 10.1111/jipb.13031
    Abstract (Browse 297)  |   Save
    Verticillium wilt diseases caused by the soil‐borne fungus Verticillium dahliae result in devastating yield losses in many economically important crops annually. Here, we identified a novel ethylene‐inducing xylanase (EIX)‐like protein, VdEIX3, from V. dahliae, which exhibits immunity‐inducing activity in Nicotiana benthamiana. In vitro‐purified VdEIX3 can induce strong oxidative burst, activate the expression of defense‐related genes, and increase resistance against oomycete and fungal pathogens in N. benthamiana. VdEIX3 orthologs of other Verticillium pathogens also induce cell death in N. benthamiana, which form a new type of EIX protein family that is distinct from the known EIX proteins. A leucine‐rich repeat receptor‐like protein, NbEIX2, regulates the perception of VdEIX3 in N. benthamiana. Our results demonstrate that VdEIX3 is a novel EIX‐like protein that can be recognized by N. benthamiana NbEIX2, and also suggest that NbEIX2 is a promising receptor‐like protein that is potentially applicable to transgenic breeding for improving resistance to Verticillium wilt diseases.
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    The novel peptide NbPPI1 identified from Nicotiana benthamiana triggers immune responses and enhances resistance against Phytophthora pathogens
    Qujiang Wen, Manli Sun, Xianglan Kong, Yang Yang, Qiang Zhang, Guiyan Huang, Wenqin Lu, Wanyue Li, Yuling Meng and Weixing Shan
    J Integr Plant Biol 2021, 63 (5): 961-976.  
    DOI: 10.1111/jipb.13033
    Abstract (Browse 321)  |   Save
    In plants, recognition of small secreted peptides, such as damage/danger‐associated molecular patterns (DAMPs), regulates diverse processes, including stress and immune responses. Here, we identified an SGPS (Ser‐Gly‐Pro‐Ser) motif‐containing peptide, Nicotiana tabacum NtPROPPI, and its two homologs in Nicotiana benthamiana, NbPROPPI1 and NbPROPPI2. Phytophthora parasitica infection and salicylic acid (SA) treatment induced NbPROPPI1/2 expression. Moreover, SignalP predicted that the 89‐amino acid NtPROPPI includes a 24‐amino acid N‐terminal signal peptide and NbPROPPI1/2‐GFP fusion proteins were mainly localized to the periplasm. Transient expression of NbPROPPI1/2 inhibited P. parasitica colonization, and NbPROPPI1/2 knockdown rendered plants more susceptible to P. parasitica. An eight‐amino‐acid segment in the NbPROPPI1 C‐terminus was essential for its immune function and a synthetic 20‐residue peptide, NbPPI1, derived from the C‐terminus of NbPROPPI1 provoked significant immune responses in N. benthamiana. These responses led to enhanced accumulation of reactive oxygen species, activation of mitogen‐activated protein kinases, and up‐regulation of the defense genes Flg22‐induced receptor‐like kinase (FRK) and WRKY DNA‐binding protein 33 (WRKY33). The NbPPI1‐induced defense responses require Brassinosteroid insensitive 1‐associated receptor kinase 1 (BAK1). These results suggest that NbPPI1 functions as a DAMP in N. benthamiana; this novel DAMP provides a potentially useful target for improving plant resistance to Pytophthora pathogens.
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    Diversity, structure and function of the coiled‐coil domains of plant NLR immune receptors
    Junzhu Wang, Meng Han and Yule Liu
    J Integr Plant Biol 2021, 63 (2): 283-296.  
    doi: 10.1111/jipb.13032
    Abstract (Browse 257)  |   Save
    Plant nucleotide‐binding, leucine‐rich repeat receptors (NLRs) perceive pathogen avirulence effectors and activate defense responses. Nucleotide‐binding, leucine‐rich repeat receptors are classified into coiled‐coil (CC)‐containing and Toll/interleukin‐1 receptor (TIR)‐containing NLRs. Recent advances suggest that NLR CC domains often function in signaling activation, especially for induction of cell death. In this review, we outline our current understanding of NLR CC domains, including their diversity/classification and structure, their roles in cell death induction, disease resistance, and interaction with other proteins. Furthermore, we provide possible directions for future work.
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    Roles of DEMETER in regulating DNA methylation in vegetative tissues and pathogen resistance
    Wenjie Zeng, Huan Huang, Xueqiang Lin, Chen Zhu, Ken‐ichi Kosami, Chaofeng Huang, Huiming Zhang, Cheng‐Guo Duan, Jian‐Kang Zhu and Daisuke Miki
    J Integr Plant Biol 2021, 63 (4): 691-706.  
    doi: 10.1111/jipb.13037
    Abstract (Browse 307)  |   Save
    DNA methylation is an epigenetic mark important for genome stability and gene expression. In Arabidopsis thaliana, the 5‐methylcytosine DNA glycosylase/demethylase DEMETER (DME) controls active DNA demethylation during the reproductive stage; however, the lethality of loss‐of‐function dme mutations has made it difficult to assess DME function in vegetative tissues. Here, we edited DME using clustered regularly interspaced short palindromic repeats (CRISPR) /CRISPR‐associated protein 9 and created three weak dme mutants that produced a few viable seeds. We also performed central cell‐specific complementation in a strong dme mutant and combined this line with mutations in the other three Arabidopsis demethylase genes to generate the dme ros1 dml2 dml3 (drdd) quadruple mutant. A DNA methylome analysis showed that DME is required for DNA demethylation at hundreds of genomic regions in vegetative tissues. A transcriptome analysis of the drdd mutant revealed that DME and the other three demethylases are important for plant responses to biotic and abiotic stresses in vegetative tissues. Despite the limited role of DME in regulating DNA methylation in vegetative tissues, the dme mutants showed increased susceptibility to bacterial and fungal pathogens. Our study highlights the important functions of DME in vegetative tissues and provides valuable genetic tools for future investigations of DNA demethylation in plants.
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    The Class III peroxidase gene OsPrx30, transcriptionally modulated by the AT‐hook protein OsATH1, mediates rice bacterial blight‐induced ROS accumulation
    Hao Liu, Shuangyu Dong, Ming Li, Fengwei Gu, Guili Yang, Tao Guo, Zhiqiang Chen and Jiafeng Wang
    J Integr Plant Biol 2021, 63 (2): 393-408.  
    doi: 10.1111/jipb.13040
    Abstract (Browse 439)  |   Save
    Class III peroxidases (CIII Prxs) play critical roles in plant immunity by scavenging reactive oxygen species (ROS). However, the functions of CIII Prxs in rice (Oryza sativa L.) immunity are largely unexplored. Here, we report a Prx precursor, OsPrx30, that is responsive to the bacterial blight Xanthomonas oryzae pv. oryzae (Xoo). OsPrx30 was primarily expressed in rice roots, leaves, and stems, and its protein product was mainly localized at the endoplasmic reticulum. Overexpression of OsPrx30 enhanced the plant's susceptibility to Xoo by maintaining a high level of peroxidase (POD) activity and reducing the content of H2O2, whereas depletion of OsPrx30 had the opposite effects. Furthermore, we identified an AT‐hook transcription factor, OsATH1, that is specifically bound to the OsPrx30 promoter. As observed in plants overexpressing OsPrx30, depletion of OsATH1 enhanced susceptibility to Xoo. Finally, we demonstrated that depletion of OsATH1 increased histone H3 acetylation at the AT‐rich region of the OsPrx30 promoter. Taken together, these results reveal a mechanism underlying the POD‐induced natural resistance to bacterial diseases and suggest a model for transcription regulation of Prx genes in rice.
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    The NPR1‐WRKY46‐WRKY6 signaling cascade mediates probenazole/salicylic acid‐elicited leaf senescence in Arabidopsis thaliana
    Dingyu Zhang, Zheng Zhu, Jiong Gao, Xin Zhou, Shuai Zhu, Xiaoyan Wang, Xiaolei Wang, Guodong Ren and Benke Kuai
    J Integr Plant Biol 2021, 63 (5): 924-936.  
    DOI: 10.1111/jipb.13044
    Abstract (Browse 462)  |   Save
    Endogenous salicylic acid (SA) regulates leaf senescence, but the underlying mechanism remains largely unexplored. The exogenous application of SA to living plants is not efficient for inducing leaf senescence. By taking advantage of probenazole (PBZ)‐induced biosynthesis of endogenous SA, we previously established a chemical inducible leaf senescence system that depends on SA biosynthesis and its core signaling receptor NPR1 in Arabidopsis thaliana. Here, using this system, we identified WRKY46 and WRKY6 as key components of the transcriptional machinery downstream of NPR1 signaling. Upon PBZ treatment, the wrky46 mutant exhibited significantly delayed leaf senescence. We demonstrate that NPR1 is essential for PBZ/SA‐induced WRKY46 activation, whereas WRKY46 in turn enhances NPR1 expression. WRKY46 interacts with NPR1 in the nucleus, binding to the W‐box of the WRKY6 promoter to induce its expression in response to SA signaling. Dysfunction of WRKY6 abolished PBZ‐induced leaf senescence, while overexpression of WRKY6 was sufficient to accelerate leaf senescence even under normal growth conditions, suggesting that WRKY6 may serve as an integration node of multiple leaf senescence signaling pathways. Taken together, these findings reveal that the NPR1‐WRKY46‐WRKY6 signaling cascade plays a critical role in PBZ/SA‐mediated leaf senescence in Arabidopsis.
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    Plant plasma membrane‐resident receptors: Surveillance for infections and coordination for growth and development
    Ana Marcia Escocard de Azevedo Manhães, Fausto Andres Ortiz‐Morea, Ping He and Libo Shan
    J Integr Plant Biol 2021, 63 (1): 79-101.  
    doi: 10.1111/jipb.13051
    Abstract (Browse 336)  |   Save
    As sessile organisms, plants are exposed to pathogen invasions and environmental fluctuations. To overcome the challenges of their surroundings, plants acquire the potential to sense endogenous and exogenous cues, resulting in their adaptability. Hence, plants have evolved a large collection of plasma membrane‐resident receptors, including RECEPTOR‐LIKE KINASEs (RLKs) and RECEPTOR‐LIKE PROTEINs (RLPs) to perceive those signals and regulate plant growth, development, and immunity. The ability of RLKs and RLPs to recognize distinct ligands relies on diverse categories of extracellular domains evolved. Co‐regulatory receptors are often required to associate with RLKs and RLPs to facilitate cellular signal transduction. RECEPTOR‐LIKE CYTOPLASMIC KINASEs (RLCKs) also associate with the complex, bifurcating the signal to key signaling hubs, such as MITOGEN‐ACTIVATED PROTEIN KINASE (MAPK) cascades, to regulate diverse biological processes. Here, we discuss recent knowledge advances in understanding the roles of RLKs and RLPs in plant growth, development, and immunity, and their connection with co‐regulatory receptors, leading to activation of diverse intracellular signaling pathways.
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    Phyllosphere microbiota: Community dynamics and its interaction with plant hosts
    Tianyu Gong and Xiu‐Fang Xin
    J Integr Plant Biol 2021, 63 (2): 297-304.  
    doi: 10.1111/jipb.13060
    Abstract (Browse 627)  |   Save
    Plants are colonized by various microorganisms in natural environments. While many studies have demonstrated key roles of the rhizosphere microbiota in regulating biological processes such as nutrient acquisition and resistance against abiotic and biotic challenges, less is known about the role of the phyllosphere microbiota and how it is established and maintained. This review provides an update on current understanding of phyllosphere community assembly and the mechanisms by which plants and microbes establish the phyllosphere microbiota for plant health.
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    Comprehensive identification of lysine 2‐hydroxyisobutyrylated proteins in Ustilaginoidea virens reveals the involvement of lysine 2‐hydroxyisobutyrylation in fungal virulence
    Xiaoyang Chen, Xiabing Li, Pingping Li, Xiaolin Chen, Hao Liu, Junbin Huang, Chaoxi Luo, Tom Hsiang and Lu Zheng
    J Integr Plant Biol 2021, 63 (2): 409-425.  
    doi: 10.1111/jipb.13066
    Abstract (Browse 461)  |   Save
    Lysine 2‐hydroxyisobutyrylation (Khib) is a newly identified post‐translational modification (PTM) that plays important roles in transcription and cell proliferation in eukaryotes. However, its function remains unknown in phytopathogenic fungi. Here, we performed a comprehensive assessment of Khib in the rice false smut fungus Ustilaginoidea virens, using Tandem Mass Tag (TMT)‐based quantitative proteomics approach. A total of 3 426 Khib sites were identified in 977 proteins, suggesting that Khib is a common and complex PTM in U. virens. Our data demonstrated that the 2‐hydroxyisobutyrylated proteins are involved in diverse biological processes. Network analysis of the modified proteins revealed a highly interconnected protein network that included many well‐studied virulence factors. We confirmed that the Zn‐binding reduced potassium dependency3‐type histone deacetylase (UvRpd3) is a major enzyme that removes 2‐hydroxyisobutyrylation and acetylation in U. virens. Notably, mutations of Khib sites in the mitogen‐activated protein kinase (MAPK) UvSlt2 significantly reduced fungal virulence and decreased the enzymatic activity of UvSlt2. Molecular dynamics simulations demonstrated that 2‐hydroxyisobutyrylation in UvSlt2 increased the hydrophobic solvent‐accessible surface area and thereby affected binding between the UvSlt2 enzyme and its substrates. Our findings thus establish Khib as a major post‐translational modification in U. virens and point to an important role for Khib in the virulence of this phytopathogenic fungus.
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    The Phytophthora effector Avh241 interacts with host NDR1-like proteins to manipulate plant immunity
    Bo Yang, Sen Yang, Baodian Guo, Yuyin Wang, Wenyue Zheng, Mengjun Tian, Kaixin Dai, Zehan Liu, Haonan Wang, Zhenchuan Ma, Yan Wang, Wenwu Ye, Suomeng Dong and Yuanchao Wang
    J Integr Plant Biol 2021, 63 (7): 1382-1396.  
    DOI: 10.1111/jipb.13082
    Abstract (Browse 339)  |   Save
    Plant pathogens rely on effector proteins to suppress host innate immune responses and facilitate colonization. Although the Phytophthora sojae RxLR effector Avh241 promotes Phytophthora infection, the molecular basis of Avh241 virulence remains poorly understood. Here we identified non-race specific disease resistance 1 (NDR1)-like proteins, the critical components in plant effector-triggered immunity (ETI) responses, as host targets of Avh241. Avh241 interacts with NDR1 in the plasma membrane and suppresses NDR1-participated ETI responses. Silencing of GmNDR1s increases the susceptibility of soybean to P. sojae infection, and overexpression of GmNDR1s reduces infection, which supports its positive role in plant immunity against P. sojae. Furthermore, we demonstrate that GmNDR1 interacts with itself, and Avh241 probably disrupts the self-association of GmNDR1. These data highlight an effective counter-defense mechanism by which a Phytophthora effector suppresses plant immune responses, likely by disturbing the function of NDR1 during infection.
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    Ustilaginoidea virens modulates lysine 2-hydroxyisobutyrylation in rice flowers during infection
    Xiaoyang Chen, Qiutao Xu, Yuhang Duan, Hao Liu, Xiaolin Chen, Junbin Huang, Chaoxi Luo, Dao‐Xiu Zhou and Lu Zheng
    J Integr Plant Biol 2021, 63 (10): 1801-1814.  
    doi: 10.1111/jipb.13149
    Abstract (Browse 298)  |   Save
    The post-translational modification lysine 2-hydroxyisobutyrylation (Khib) plays an important role in gene transcription, metabolism, and enzymatic activity. Khib sites have been identified in rice (Oryza sativa). However, the Khib status of proteins in rice flowers during pathogen infection remains unclear. Here, we report a comprehensive identification of Khib-modified proteins in rice flowers, and the changes in these proteins during infection with the fungal pathogen Ustilaginoidea virens. By using a tandem mass tag-based quantitative proteomics approach, we identified 2,891 Khib sites on 964 proteins in rice flowers. Our data demonstrated that 2-hydroxyisobutyrylated proteins are involved in diverse biological processes. Khib levels were substantially reduced upon infection with U. virens. Chromatin immunoprecipitation polymerase chain reaction (PCR) and reverse transcription quantitative PCR analyses revealed that histone Khib is involved in the expression of disease-resistance genes. More importantly, most quantified sites on core histones H3 were downregulated upon U. virens infection. In addition, the histone deacetylases HDA705, HDA716, SRT1, and SRT2 are involved in the removal of Khib marks in rice. HDA705 was further confirmed to negatively regulate rice disease resistance to pathogens U. virens, Magnaporthe oryzae, and Xanthomonas oryzae pv. oryzae (Xoo). Our data suggest that U. virens could modulate Khib in rice flowers during infection.
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    Drought stress and plant ecotype drive microbiome recruitment in switchgrass rhizosheath
    Tie‐Yuan Liu, Nenghui Ye, Xinyu Wang, Debatosh Das, Yuxiang Tan, Xiangkai You, Mingxiu Long, Tianming Hu, Lei Dai, Jianhua Zhang and Mo‐Xian Chen
    J Integr Plant Biol 2021, 63 (10): 1753-1774.  
    doi: 10.1111/jipb.13154
    Abstract (Browse 296)  |   Save
    The rhizosheath, a layer of soil grains that adheres firmly to roots, is beneficial for plant growth and adaptation to drought environments. Switchgrass is a perennial C4 grass which can form contact rhizosheath under drought conditions. In this study, we characterized the microbiomes of four different rhizocompartments of two switchgrass ecotypes (Alamo and Kanlow) grown under drought or well-watered conditions via 16S ribosomal RNA amplicon sequencing. These four rhizocompartments, the bulk soil, rhizosheath soil, rhizoplane, and root endosphere, harbored both distinct and overlapping microbial communities. The root compartments (rhizoplane and root endosphere) displayed low-complexity communities dominated by Proteobacteria and Firmicutes. Compared to bulk soil, Cyanobacteria and Bacteroidetes were selectively enriched, while Proteobacteria and Firmicutes were selectively depleted, in rhizosheath soil. Taxa from Proteobacteria or Firmicutes were specifically selected in Alamo or Kanlow rhizosheath soil. Following drought stress, Citrobacter and Acinetobacter were further enriched in rhizosheath soil, suggesting that rhizosheath microbiome assembly is driven by drought stress. Additionally, the ecotype-specific recruitment of rhizosheath microbiome reveals their differences in drought stress responses. Collectively, these results shed light on rhizosheath microbiome recruitment in switchgrass and lay the foundation for the improvement of drought tolerance in switchgrass by regulating the rhizosheath microbiome.
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    Balancing selection and wild gene pool contribute to resistance in global rice germplasm against planthopper
    Cong Zhou, Qian Zhang, Yu Chen, Jin Huang, Qin Guo, Yi Li, Wensheng Wang, Yongfu Qiu, Wei Guan, Jing Zhang, Jianping Guo, Shaojie Shi, Di Wu, Xiaohong Zheng, Lingyun Nie, Jiaoyan Tan, Chaomei Huang, Yinhua Ma, Fang Yang, Xiqin Fu, Bo Du, Lili Zhu, Rongzhi Chen, Zhikang Li, Longping Yuan and Guangcun He
    J Integr Plant Biol 2021, 63 (10): 1695-1711.  
    doi: 10.1111/jipb.13157
    Abstract (Browse 330)  |   Save
    Interactions and co-evolution between plants and herbivorous insects are critically important in agriculture. Brown planthopper (BPH) is the most severe insect of rice, and the biotypes adapt to feed on different rice genotypes. Here, we present genomics analyses on 1,520 global rice germplasms for resistance to three BPH biotypes. Genome-wide association studies identified 3,502 single nucleotide polymorphisms (SNPs) and 59 loci associated with BPH resistance in rice. We cloned a previously unidentified gene Bph37 that confers resistance to BPH. The associated loci showed high nucleotide diversity. Genome-wide scans for trans-species polymorphisms revealed ancient balancing selection at the loci. The secondarily evolved insect biotypes II and III exhibited significantly higher virulence and overcame more rice varieties than the primary biotype I. In response, more SNPs and loci evolved in rice for resistance to biotypes II and III. Notably, three exceptional large regions with high SNP density and resistance-associated loci on chromosomes 4 and 6 appear distinct between the resistant and susceptible rice varieties. Surprisingly, these regions in resistant rice might have been retained from wild species Oryza nivara. Our findings expand the understanding of long-term interactions between rice and BPH and provide resistance genes and germplasm resources for breeding durable BPH-resistant rice varieties.
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    Versatile effectors of phytopathogenic fungi target host immunity
    Muhammad Tariqjaveed, Abdul Mateen, Shanzhi Wang, Shanshan Qiu, Xinhang Zheng, Jie Zhang, Vijai Bhadauria and Wenxian Sun
    J Integr Plant Biol 2021, 63 (11): 1856-1873.  
    DOI: 10.1111/jipb.13162
    Abstract (Browse 379)  |   Save
    Phytopathogenic fungi secrete a large arsenal of effector molecules, including proteinaceous effectors, small RNAs, phytohormones and derivatives thereof. The pathogenicity of fungal pathogens is primarily determined by these effectors that are secreted into host cells to undermine innate immunity, as well as to facilitate the acquisition of nutrients for their in planta growth and proliferation. After conventional and non-conventional secretion, fungal effectors are translocated into different subcellular compartments of the host cells to interfere with various biological processes. In extracellular spaces, apoplastic effectors cope with physical and chemical barriers to break the first line of plant defenses. Intracellular effectors target essential immune components on the plasma membrane, in the cytosol, including cytosolic organelles, and in the nucleus to suppress host immunity and reprogram host physiology, favoring pathogen colonization. In this review, we comprehensively summarize the recent advances in fungal effector biology, with a focus on the versatile virulence functions of fungal effectors in promoting pathogen infection and colonization. A perspective of future research on fungal effector biology is also discussed.
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