Journal of Genetics and Genomics

From plant immunity to crop disease resistance

Yan Zhao, Xiaobo Zhu, Xuewei Chen, Jian-Min Zhou

2022, 49(8): 693-703. doi: 10.1016/j.jgg.2022.06.003

Abstract (778) PDF (87)

Abstract:
Plant diseases caused by diverse pathogens lead to a serious reduction in crop yield and threaten food security worldwide. Genetic improvement of plant immunity is considered as the most effective and sustainable approach to control crop diseases. In the last decade, our understanding of plant immunity at both molecular and genomic levels has improved greatly. Combined with advances in biotechnologies, particularly clustered regularly interspaced short palindromic repeat (CRISPR)/Cas9-based genome editing, we can now rapidly identify new resistance genes and engineer disease-resistance crop plants like never before. In this review, we summarize the current knowledge of plant immunity and outline existing and new strategies for disease resistance improvement in crop plants. We also discuss existing challenges in this field and suggest directions for future studies.

Regulation and integration of plant jasmonate signaling: a comparative view of monocot and dicot

Shiwei Wan, Xiu-Fang Xin

2022, 49(8): 704-714. doi: 10.1016/j.jgg.2022.04.002

Abstract (786) PDF (109)

Abstract:
The phytohormone jasmonate plays a pivotal role in various aspects of plant life, including developmental programs and defense against pests and pathogens. A large body of knowledge on jasmonate biosynthesis, signal transduction as well as its functions in diverse plant processes has been gained in the past two decades. In addition, there exists extensive crosstalk between jasmonate pathway and other phytohormone pathways, such as salicylic acid (SA) and gibberellin (GA), in co-regulation of plant immune status, fine-tuning the balance of plant growth and defense, and so on, which were mostly learned from studies in the dicotyledonous model plants Arabidopsis thaliana and tomato but much less in monocot. Interestingly, existing evidence suggests both conservation and functional divergence in terms of core components of jasmonate pathway, its biological functions and signal integration with other phytohormones, between monocot and dicot. In this review, we summarize the current understanding on JA signal initiation, perception and regulation, and highlight the distinctive characteristics in different lineages of plants.

The molecular mechanism of plasma membrane H⁺-ATPases in plant responses to abiotic stress

Jing Li, Yan Guo, Yongqing Yang

2022, 49(8): 715-725. doi: 10.1016/j.jgg.2022.05.007

Abstract (770) PDF (59)

Abstract:
Plasma membrane H⁺-ATPases (PM H⁺-ATPases) are critical proton pumps that export protons from the cytoplasm to the apoplast. The resulting proton gradient and difference in electrical potential energize various secondary active transport events. PM H⁺-ATPases play essential roles in plant growth, development, and stress responses. In this review, we focus on recent studies of the mechanism of PM H⁺-ATPases in response to abiotic stresses in plants, such as salt and high pH, temperature, drought, light, macronutrient deficiency, acidic soil and aluminum stress, as well as heavy metal toxicity. Moreover, we discuss remaining outstanding questions about how PM H⁺-ATPases contribute to abiotic stress responses.

Emerging roles of phosphoinositide-associated membrane trafficking in plant stress responses

Feng Lin, Junming Zheng, Yanhua Xie, Wen Jing, Qun Zhang, Wenhua Zhang

2022, 49(8): 726-734. doi: 10.1016/j.jgg.2022.05.003

Abstract (375) PDF (38)

Abstract:
Eukaryotic cells are confined by membranes that create hydrophobic barriers for substance and information exchange between the inside and outside of the cell. These barriers are formed by assembly of lipids and protein in aqueous environments. Lipids not only serve as building blocks for membrane construction, but also possess regulatory functions in cellular activities. These regulatory lipids are non-uniformly distributed in membrane systems; their temporal and spatial accumulation in specific membranes decodes environmental cues and changes cellular activity accordingly. Phosphoinositides (PIs) are phospholipids that exert regulatory effects. In recent years, research on PIs roles in regulating plant growth, development, and responses to environmental stress is increasing. Several reviews have been published on the composition of PIs, intermolecular transferring of PIs by lipid kinases (phosphatases) or PI-PLCs, subcellular localization, and specially their functions in plant developments. Herein, we review the crucial regulatory functions of PIs in plant stress responses, with a particular focus on PIs involved in membrane trafficking.

Plants response to light stress

Yafei Shi, Xiangsheng Ke, Xiaoxia Yang, Yuhan Liu, Xin Hou

2022, 49(8): 735-747. doi: 10.1016/j.jgg.2022.04.017

Abstract (722) PDF (122)

Abstract:
Plants require solar energy to grow through oxygenic photosynthesis; however, when light intensity exceeds the optimal range for photosynthesis, it causes abiotic stress and physiological damage in plants. In response to high light stress, plants initiate a series of signal transduction from chloroplasts to whole cells and from locally stressed tissues to the rest of the plant body. These signals trigger a variety of physiological and biochemical reactions intended to mitigate the deleterious effects of high light intensity, such as photodamage and photoinhibition. Light stress protection mechanisms include chloroplastic Reactive oxygen species (ROS) scavenging, chloroplast and stomatal movement, and anthocyanin production. Photosynthetic apparatuses, being the direct targets of photodamage, have also developed various acclimation processes such as thermal energy dissipation through nonphotochemical quenching (NPQ), photorepair of Photosystem II (PSII), and transcriptional regulation of photosynthetic proteins. Fluctuating light is another mild but persistent type of light stress in nature, which unfortunately has been poorly investigated. Current studies, however, suggest that state transitions and cyclic electron transport are the main adaptive mechanisms for mediating fluctuating light stress in plants. Here, we review the current breadth of knowledge regarding physiological and biochemical responses to both high light stress and fluctuating light stress.

Abiotic stress-triggered oxidative challenges: Where does H₂S act?

Linda de Bont, Xiujie Mu, Bo Wei, Yi Han

2022, 49(8): 748-755. doi: 10.1016/j.jgg.2022.02.019

Abstract (183) PDF (9)

Abstract:
Hydrogen sulfide (H₂S) was once principally considered the perpetrator of plant growth cessation and cell death. However, this has become an antiquated view, with cumulative evidence showing that the H₂S serves as a biological signaling molecule notably involved in abiotic stress response and adaptation, such as defense by phytohormone activation, stomatal movement, gene reprogramming, and plant growth modulation. Reactive oxygen species (ROS)-dependent oxidative stress is involved in these responses. Remarkably, an ever-growing body of evidence indicates that H₂S can directly interact with ROS processing systems in a redox-dependent manner, while it has been gradually recognized that H₂S-based posttranslational modifications of key protein cysteine residues determine stress responses. Furthermore, the reciprocal interplay between H₂S and nitric oxide (NO) in regulating oxidative stress has significant importance. The interaction of H₂S with NO and ROS during acclimation to abiotic stress may vary from synergism to antagonism. However, the molecular pathways and factors involved remain to be identified. This review not only aims to provide updated information on H₂S action in regulating ROS-dependent redox homeostasis and signaling, but also discusses the mechanisms of H₂S-dependent regulation in the context of oxidative stress elicited by environmental cues.

Nitric oxide negatively regulates gibberellin signaling to coordinate growth and salt tolerance in Arabidopsis

Lichao Chen, Shuhao Sun, Chun-Peng Song, Jian-Min Zhou, Jiayang Li, Jianru Zuo

2022, 49(8): 756-765. doi: 10.1016/j.jgg.2022.02.023

Abstract (196) PDF (33)

Abstract:
In response to dynamically altered environments, plants must finely coordinate the balance between growth and stress responses for their survival. However, the underpinning regulatory mechanisms remain largely elusive. The phytohormone gibberellin promotes growth via a derepression mechanism by proteasomal degradation of the DELLA transcription repressors. Conversely, the stress-induced burst of nitric oxide (NO) enhances stress tolerance, largely relying on NO-mediated S-nitrosylation, a redox-based posttranslational modification. Here, we show that S-nitrosylation of Cys-374 in the Arabidopsis RGA protein, a key member of DELLAs, inhibits its interaction with the F-box protein SLY1, thereby preventing its proteasomal degradation under salinity condition. The accumulation of RGA consequently retards growth but enhances salt tolerance. We propose that NO negatively regulates gibberellin signaling via S-nitrosylation of RGA to coordinate the balance of growth and stress responses when challenged by adverse environments.

OsMPK4 promotes phosphorylation and degradation of IPA1 in response to salt stress to confer salt tolerance in rice

Meiru Jia, Nan Luo, Xiangbing Meng, Xiaoguang Song, Yanhui Jing, Liquan Kou, Guifu Liu, Xiahe Huang, Yingchun Wang, Jiayang Li, Bing Wang, Hong Yu

2022, 49(8): 766-775. doi: 10.1016/j.jgg.2022.06.009

Abstract (566) PDF (163)

Abstract:
Salt stress adversely affects plant growth, development, and crop yield. Rice (Oryza sativa L.) is one of the most salt-sensitive cereal crops, especially at the early seedling stage. Mitogen-activated protein kinase (MAPK/MPK) cascades have been shown to play critical roles in salt response in Arabidopsis. However, the roles of the MPK cascade signaling in rice salt response and substrates of OsMPK remain largely unknown. Here, we report that the salt-induced OsMPK4-Ideal Plant Architecture 1 (IPA1) signaling pathway regulates the salt tolerance in rice. Under salt stress, OsMPK4 could interact with IPA1 and phosphorylate IPA1 at Thr180, leading to degradation of IPA1. Genetic evidence shows that IPA1 is a negative regulator of salt tolerance in rice, whereas OsMPK4 promotes salt response in an IPA1-dependent manner. Taken together, our results uncover an OsMPK4-IPA1 signal cascade that modulates the salt stress response in rice and sheds new light on the breeding of salt-tolerant rice varieties.

Function of hydroxycinnamoyl transferases for the biosynthesis of phenolamides in rice resistance to Magnaporthe oryzae

Hong Fang, Fan Zhang, Chongyang Zhang, Dan Wang, Shuangqian Shen, Feng He, Hui Tao, Ruyi Wang, Min Wang, Debao Wang, Xionglun Liu, Jie Luo, Guo-Liang Wang, Yuese Ning

2022, 49(8): 776-786. doi: 10.1016/j.jgg.2022.02.008

Abstract (429) PDF (24)

Abstract:
Phenolamide (PA) metabolites play important roles in the interaction between plants and pathogens. The putrescine hydroxycinnamoyl transferase genes OsPHT3 and OsPHT4 positively regulate rice cell death and resistance to Magnaporthe oryzae. The bZIP transcription factor APIP5, a negative regulator of cell death and rice immunity, directly binds to the OsPHT4 promoter to regulate putrescine-derived PAs. Whether other hydroxycinnamoyl transferase (HT) genes also participate in APIP5-mediated immunity remains unclear. Surprisingly, we find that genes encoding agmatine hydroxycinnamoyl transferases OsAHT1 and OsAHT2, tryptamine hydroxycinnamoyl transferases OsTBT1 and OsTBT2, and tyramine hydroxycinnamoyl transferases OsTHT1 and OsTHT2, responsible for the biosynthesis of polyamine-derived PAs are all up-regulated in APIP5-RNAi transgenic plants compared with segregated wild-type rice. Furthermore, both OsAHT1/2 and OsTBT1/2 are induced during M.oryzae infection, showing expression patterns similar to those previously reported for OsTHT1/2 and OsPHT3/4. Transgenic plants overexpressing either OsAHT2-GFP or OsTBT1-GFP show enhanced resistance against M.oryzae and accumulated more PA metabolites and lignin compared with wild-type plants. Interestingly, as demonstrated for OsPHT4, APIP5 directly binds to the promoters of OsAHT1/2, OsTBT1/2, and OsTHT1/2, repressing their transcription. Together, these results indicate that the HT genes are common targets of APIP5 and that PAs play critical roles in rice immunity.

Functional characterization of powdery mildew resistance gene MlIW172, a new Pm60 allele and its allelic variation in wild emmer wheat

Qiuhong Wu, Yongxing Chen, Beibei Li, Jing Li, Panpan Zhang, Jingzhong Xie, Huaizhi Zhang, Guanghao Guo, Ping Lu, Miaomiao Li, Keyu Zhu, Wenling Li, Tzion Fahima, Eviatar Nevo, Hongjie Li, Lingli Dong, Zhiyong Liu

2022, 49(8): 787-795. doi: 10.1016/j.jgg.2022.01.010

Abstract (463) PDF (51)

Abstract:
Wild emmer wheat (Triticum dicoccoides, WEW) is an immediate progenitor of both the cultivated tetraploid and hexaploid wheats and it harbors rich genetic diversity against powdery mildew caused by Blumeria graminis f. sp. tritici (Bgt). A powdery mildew resistance gene MlIW172 originated from WEW accession IW172 (G-797-M) is fine mapped in a 0.048 centimorgan (cM) genetic interval on 7AL, corresponding to a genomic region spanning 233kb, 1Mb and 800kb in Chinese Spring, WEW Zavitan, and T.urartu G1812, respectively. MlIW172 encodes a typical NLR protein NLR^IW172 and physically locates in an NBS-LRR gene cluster. NLR is subsequently identified as a new allele of Pm60, and its function is validated by EMS mutagenesis and transgenic complementation. Haplotype analysis of the Pm60 alleles reveals diversifications in sequence variation in the locus and presence and absence variations (PAV) in WEW populations. Four common single nucleotide variations (SNV) are detected between the Pm60 alleles from WEW and T.urartu, indicative of speciation divergence between the two different wheat progenitors. The newly identified Pm60 alleles and haplotypes in WEW are anticipated to be valuable for breeding powdery mildew resistance wheat cultivars via marker-assisted selection.

Active DNA demethylation regulates MAMP-triggered immune priming in Arabidopsis

Mengling Huang, Ying Zhang, Ying Wang, Jiatao Xie, Jiasen Cheng, Yanping Fu, Daohong Jiang, Xiao Yu, Bo Li

2022, 49(8): 796-809. doi: 10.1016/j.jgg.2022.02.021

Abstract (160) PDF (17)

Abstract:
Plants recognize microbe-associated molecular patterns (MAMPs) to activate immune responses and defense priming to defend against pathogen infections. Transcriptional regulation of gene expression is crucial for plant immunity and is mediated by multiple factors, including DNA methylation. However, it remains unknown whether and how DNA demethylation contributes to immune responses in MAMP-triggered immunity. Here, we report that active DNA demethylation is required for MAMP-triggered immunity to bacterial pathogens. The rdd-2 triple mutant carrying mutations in ROS1, DML2, and DML3 that encode DNA glycosylases, which are key DNA demethylation enzymes, exhibits compromised immune responses triggered by the MAMPs flg22 and elf18. Genome-wide methylome analysis reveals that flg22 induces rapid and specific DNA demethylation in an RDD-dependent manner. The expression levels of salicylic acid signaling-related and phytoalexin biosynthesis-related genes are tightly associated with the flg22-induced promoter demethylation. The compromised accumulation of priming compounds and antimicrobial metabolites ultimately leads to a defense priming defect in the rdd-2 mutant. Our results reveal the critical role of active DNA demethylation in the MAMP-triggered immune response and provide unique insight into the molecular mechanism of flg22-modulated DNA demethylation.

Phosphorylation of an ethylene response factor by MPK3/MPK6 mediates negative feedback regulation of pathogen-induced ethylene biosynthesis in Arabidopsis

Xiaoyang Wang, Huicong Meng, Yuxi Tang, Yashi Zhang, Yunxia He, Jinggeng Zhou, Xiangzong Meng

2022, 49(8): 810-822. doi: 10.1016/j.jgg.2022.04.012

Abstract (438) PDF (48)

Abstract:
Plants under pathogen attack produce high levels of the gaseous phytohormone ethylene to induce plant defense responses via the ethylene signaling pathway. The 1-aminocyclopropane-1-carboxylate synthase (ACS) is a critical rate-limiting enzyme of ethylene biosynthesis. Transcriptional and post-translational upregulation of ACS2 and ACS6 by the mitogen-activated protein kinases MPK3 and MPK6 are previously shown to be crucial for pathogen-induced ethylene biosynthesis in Arabidopsis. Here, we report that the fungal pathogen Botrytis cinerea-induced ethylene biosynthesis in Arabidopsis is under the negative feedback regulation by ethylene signaling pathway. The ethylene response factor ERF1A is further found to act downstream of ethylene signaling to negatively regulate the B. cinerea-induced ethylene biosynthesis via indirectly suppressing the expression of ACS2 and ACS6. Interestingly, ERF1A is shown to also upregulate defensin genes directly and therefore promote Arabidopsis resistance to B.cinerea. Furthermore, ERF1A is identified to be a substrate of MPK3 and MPK6, which phosphoactivate ERF1A to enhance its functions in suppressing ethylene biosynthesis and inducing defensin gene expression. Taken together, our data reveal that ERF1A and its phosphorylation by MPK3/MPK6 not only mediate the negative-feedback regulation of the B.cinerea-induced ethylene biosynthesis, but also upregulate defensin gene expression to increase Arabidopsis resistance to B. cinerea.

Two plant NLR proteins confer strain-specific resistance conditioned by an effector from Pseudomonas syringae pv. actinidiae

Xiaojuan Zheng, Zhaoyang Zhou, Zhen Gong, Meijuan Hu, Ye Jin Ahn, Xiaojuan Zhang, Yan Zhao, Guoshu Gong, Jian Zhang, Jianru Zuo, Guan-Zhu Han, Sohn Kee Hoon, Jian-Min Zhou

2022, 49(8): 823-832. doi: 10.1016/j.jgg.2022.06.006

Abstract (288) PDF (28)

Abstract:
Pseudomonas syringae pv. actinidiae (Psa) causes bacterial canker, a devastating disease threatening the Actinidia fruit industry. In a search for non-host resistance genes against Psa, we find that the nucleotide-binding leucine-rich repeat receptor (NLR) protein ZAR1 from both Arabidopsis and Nicotiana benthamiana (Nb) recognizes HopZ5 and triggers cell death. The recognition requires ZED1 in Arabidopsis and JIM2 in Nb plants, which are members of the ZRK pseudokinases and known components of the ZAR1 resistosome. Surprisingly, Arabidopsis ZAR1 and RPM1, another NLR known to recognize HopZ5, confer disease resistance to HopZ5 in a strain-specific manner. Thus, ZAR1, but not RPM1, is solely required for resistance to P.s. maculicola ES4326 (Psm) carrying hopZ5, whereas RPM1 is primarily required for resistance to P.s. tomato DC3000 (Pst) carrying hopZ5. Furthermore, the ZAR1-mediated resistance to Psm hopZ5 in Arabidopsis is insensitive to SOBER1, which encodes a deacetylase known to suppress the RPM1-mediated resistance to Pst hopZ5. In addition, hopZ5 enhances P.syringae virulence in the absence of ZAR1 or RPM1 and that SOBER1 abolishes such virulence function. Together the study suggests that ZAR1 may be used for improving Psa resistance in Actinidia and uncovers previously unknown complexity of effector-triggered immunity and effector-triggered virulence.

2022 Vol. 49, No. 8