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Authors: Lu Liu, Yanzhi Liu, Xuehan Ji, Xia Zhao, Jun Liu and Ning Xu.
The Plant Journal (2024)
Significance Statement: Bacterial pathogens secret coronatine (COR) to recruit an importin β protein SAD2 for interfering ABA signaling in stomata and promote invasion.
Abstract: "Stomatal immunity plays an important role during bacterial pathogen invasion. Abscisic acid (ABA) induces plants to close their stomata and halt pathogen invasion, but many bacterial pathogens secrete phytotoxin coronatine (COR) to antagonize ABA signaling and reopen the stomata to promote infection at early stage of invasion. However, the underlining mechanism is not clear. SAD2 is an importin β family protein, and the sad2 mutant shows hypersensitivity to ABA. We discovered ABI1, which negatively regulated ABA signaling and reduced plant sensitivity to ABA, was accumulated in the plant nucleus after COR treatment. This event required SAD2 to import ABI1 to the plant nucleus. Abolition of SAD2 undermined ABI1 accumulation. Our study answers the long-standing question of how bacterial COR antagonizes ABA signaling and reopens plant stomata during pathogen invasion."
Authors: Ruolin Wang, Beibei Li, Jiang Zhang and Ling Chang.
PLoS ONE (2024)
Abstract: "In our previous work, cytokinin (CK) signaling and biosynthesis were found to be modulated during Arabidopsis defense against infection by the necrotrophic pathogen Botrytis cinerea. Notably, the expression level of CYTOKININ OXIDASE/DEHYDROGENASE 5 (CKX5) was significantly induced in B. cinerea-infected leaves and later in distant B. cinerea-untreated leaves of the same plant. To confirm and determine how CKX5 is involved in the response to B. cinerea infection, transcript levels of CKX family genes were analyzed in B. cinerea-inoculated leaves, and only CKX5 was remarkably induced by B. cinerea infection. Furthermore, CKX5-overexpressing Arabidopsis plants were more resistant to B. cinerea than wild-type plants. Transcription factors (TFs) binding to the CKX5 promoter were then screened by yeast one-hybrid assays. Quantitative Real-Time Reverse Transcription PCR (qRT-PCR) analysis further showed that genes encoding TFs, including WRKY40, WRKY33, ERF6, AHL15, AHL17, ANAC003, TCP13 and ANAC019, were also strongly induced in infected leaves, similar to CKX5. Analysis of ERF6-overexpressing plants and ERF6-and AHL15-knockout mutants indicated that ERF6 and AHL15 are involved in plant immunity to B. cinerea. Furthermore, CKX5 upregulation by B. cinerea infection was affected when ERF6 or AHL15 levels were altered. Our work suggests that CKX5 levels are controlled by the plant defense system to defend against attack by the pathogen B. cinerea."
Authors: Tak Lee, Martina Orvosova, Morgane Batzenschlager, Marcelo Bueno Batista, Paul C. Bailey, Nadia A. Mohd-Radzman, Aram Gurzadyan, Naomi Stuer, Kirankumar S. Mysore, Jiangqi Wen, Thomas Ott, Giles E.D. Oldroyd and Katharina Schiessl.
Current Biology (2024)
Editor's view: To host N-fixing bacteria, legumes grow root nodules initiated via a lateral root program. Lee et al. show that two LSH transcription factors mediate the divergence between lateral roots and nodules by promoting the proliferation of colonizable cells. LSH1/LSH2 regulate the nodule identity genes NF-YA1 and NOOT1/NOOT2 and auxin/cytokinin dynamics.
Highlights: • LSHs are key regulators of symbiotic root nodule differentiation downstream of NIN • LSHs promote cell divisions in the root cortex that support bacterial colonization • LSHs promote expression of the nodule organ identity genes NOOT1/NOOT2 and NF-YA1 • LSHs repress PLETHORA root regulators and modulate auxin-cytokinin dynamics
Abstract: "Legumes produce specialized root nodules that are distinct from lateral roots in morphology and function, with nodules intracellularly hosting nitrogen-fixing bacteria. We have previously shown that a lateral root program underpins nodule initiation, but there must be additional developmental regulators that confer nodule identity. Here, we show two members of the LIGHT-SENSITIVE SHORT HYPOCOTYL (LSH) transcription factor family, predominantly known to define shoot meristem complexity and organ boundaries, function as regulators of nodule organ identity. In parallel to the root initiation program, LSH1/LSH2 recruit a program into the root cortex that mediates the divergence into nodules, in particular with cell divisions in the mid-cortex. This includes regulation of auxin and cytokinin, promotion of NODULE ROOT1/2 and Nuclear Factor YA1, and suppression of the lateral root program. A principal outcome of LSH1/LSH2 function is the production of cells able to accommodate nitrogen-fixing bacteria, a key feature unique to nodules."
Authors: Deepika Mittal, Janesh Kumar Gautam, Mahendra Varma, Amrutha Laie, Shruti Mishra, Smrutisanjita Behera and Jyothilakshmi Vadassery.
Plant, Cell & Environment (2024)
Abstract: "Jasmonic acid-isoleucine (JA-Ile) is a plant defence hormone whose cellular levels are elevated upon herbivory and regulate defence signalling. Despite their pivotal role, our understanding of the rapid cellular perception of bioactive JA-Ile is limited. This study identifies cell type-specific JA-Ile-induced Ca2+ signal and its role in self-amplification and plant elicitor peptide receptor (PEPR)-mediated signalling. Using the Ca2+ reporter, R-GECO1 in Arabidopsis, we have characterized a monophasic and sustained JA-Ile-dependent Ca2+ signature in leaf epidermal cells. The rapid Ca2+ signal is independent of positive feedback by the JA-Ile receptor, COI1 and the transporter, JAT1. Microarray analysis identified up-regulation of receptors, PEPR1 and PEPR2 upon JA-Ile treatment. The pepr1 pepr2 double mutant in R-GECO1 background exhibits impaired external JA-Ile induced Ca2+cyt elevation and impacts the canonical JA-Ile responsive genes. JA responsive transcription factor, MYC2 binds to the G-Box motif of PEPR1 and PEPR2 promoter and activates their expression upon JA-Ile treatment and in myc2 mutant, this is reduced. External JA-Ile amplifies AtPep-PEPR pathway by increasing the AtPep precursor, PROPEP expression. Our work shows a previously unknown non-canonical PEPR-JA-Ile-Ca2+-MYC2 signalling module through which plants sense JA-Ile rapidly to amplify both AtPep-PEPR and jasmonate signalling in undamaged cells."
Authors: Raul Zavaliev and Xinnian Dong.
Molecular Cell (2024)
Abstract: "Nonexpressor of pathogenesis-related genes 1 (NPR1) was discovered in Arabidopsis as an activator of salicylic acid (SA)-mediated immune responses nearly 30 years ago. How NPR1 confers resistance against a variety of pathogens and stresses has been extensively studied; however, only in recent years have the underlying molecular mechanisms been uncovered, particularly NPR1’s role in SA-mediated transcriptional reprogramming, stress protein homeostasis, and cell survival. Structural analyses ultimately defined NPR1 and its paralogs as SA receptors. The SA-bound NPR1 dimer induces transcription by bridging two TGA transcription factor dimers, forming an enhanceosome. Moreover, NPR1 orchestrates its multiple functions through the formation of distinct nuclear and cytoplasmic biomolecular condensates. Furthermore, NPR1 plays a central role in plant health by regulating the crosstalk between SA and other defense and growth hormones. In this review, we focus on these recent advances and discuss how NPR1 can be utilized to engineer resistance against biotic and abiotic stresses."
Authors: Qian Gong, Yunjing Wang, Linfang He, Fan Huang, Danfeng Zhang, Yan Wang, Xiang Wei, Meng Han, Haiteng Deng, Lan Luo, Feng Cui, Yiguo Hong and Yule Liu.
Nature (2023)
Editor's view: Aphid-transmitted viruses encode proteins that suppress the plant airborne defence response—which is triggered by volatile chemicals released by neighbouring plants after aphid attack—and the plants consequently become less repellent to aphids and more suitable for aphid survival, infestation and viral transmission.
Abstract: "Aphids transmit viruses and are destructive crop pests1. Plants that have been attacked by aphids release volatile compounds to elicit airborne defence (AD) in neighbouring plants2–5. However, the mechanism underlying AD is unclear. Here we reveal that methyl-salicylate (MeSA), salicylic acid-binding protein-2 (SABP2), the transcription factor NAC2 and salicylic acid-carboxylmethyltransferase-1 (SAMT1) form a signalling circuit to mediate AD against aphids and viruses. Airborne MeSA is perceived and converted into salicylic acid by SABP2 in neighbouring plants. Salicylic acid then causes a signal transduction cascade to activate the NAC2–SAMT1 module for MeSA biosynthesis to induce plant anti-aphid immunity and reduce virus transmission. To counteract this, some aphid-transmitted viruses encode helicase-containing proteins to suppress AD by interacting with NAC2 to subcellularly relocalize and destabilize NAC2. As a consequence, plants become less repellent to aphids, and more suitable for aphid survival, infestation and viral transmission. Our findings uncover the mechanistic basis of AD and an aphid–virus co-evolutionary mutualism, demonstrating AD as a potential bioinspired strategy to control aphids and viruses."
Authors: Xinru Huang, Weiwei Zhang, Yongling Liao, Jiabao Ye and Feng Xu.
Plant (2024)
Key message: This review summarized how TFs function independently or in response to environmental factors to regulate terpenoid biosynthesis via fine-tuning the expression of rate-limiting enzymes.
Abstract: "Terpenoids are derived from various species and sources. They are essential for interacting with the environment and defense mechanisms, such as antimicrobial, antifungal, antiviral, and antiparasitic properties. Almost all terpenoids have high medicinal value and economic performance. Recently, the control of enzyme genes on terpenoid biosynthesis has received a great deal of attention, but transcriptional factors regulatory network on terpenoid biosynthesis and accumulation has yet to get a thorough review. Transcription factors function as activators or suppressors independently or in response to environmental stimuli, fine-tuning terpenoid accumulation through regulating rate-limiting enzyme expression. This study investigates the advancements in transcription factors related to terpenoid biosynthesis and systematically summarizes previous works on the specific mechanisms of transcription factors that regulate terpenoid biosynthesis via hormone signal–transcription regulatory networks in plants. This will help us to better comprehend the regulatory network of terpenoid biosynthesis and build the groundwork for terpenoid development and effective utilization."
Authors: Shuhuan Zhang, Weihao Miao, Ye Liu, Jiafu Jiang, Sumei Chen, Fadi Chen and Zhiyong Guan.
BMC Genomics (2023)
Abstract: "Background - Black spot disease caused by the necrotrophic fungus Alternaria spp. is one of the most devastating diseases affecting Chrysanthemum morifolium. There is currently no effective way to prevent chrysanthemum black spot. Results - We revealed that pre-treatment of chrysanthemum leaves with the methyl jasmonate (MeJA) significantly reduces their susceptibility to Alternaria alternata. To understand how MeJA treatment induces resistance, we monitored the dynamics of metabolites and the transcriptome in leaves after MeJA treatment following A. alternata infection. JA signaling affected the resistance of plants to pathogens through cell wall modification, Ca2+ regulation, reactive oxygen species (ROS) regulation, mitogen‐activated protein kinase cascade and hormonal signaling processes, and the accumulation of anti-fungal and anti-oxidant metabolites. Furthermore, the expression of genes associated with these functions was verified by reverse transcription quantitative PCR and transgenic assays. Conclusion - Our findings indicate that MeJA pre-treatment could be a potential orchestrator of a broad-spectrum defense response that may help establish an ecologically friendly pest control strategy and offer a promising way of priming plants to induce defense responses against A. alternata."
Authors: Shaoqin Li, Yongping Yang, Li He, Xiao Han, Yanru Hu and Yanjuan Jiang.
bioRxiv (2023)
Abstract: "Cold stress affects plant immune responses, and this process may involve the salicylic acid (SA) signaling pathway. However, the underlying mechanism by which low temperature signals coordinate with SA signaling to regulate plant immunity remains poorly characterized. Here, we found that low temperatures enhanced the disease resistance of Arabidopsis against Pseudomonas syringae pv. tomato (Pst) DC3000. This process required Inducer of CBF expression 1 (ICE1), the core transcription factor in cold-signal cascades. ICE1 physically interacted with Non-expresser of PR genes 1 (NPR1), the master regulator of the SA signaling pathway. Enrichment of ICE1 on the PR1 promoter and its ability to transcriptionally activate PR1 were enhanced by NPR1. Further analyses revealed that cold stress signals cooperate with SA signals to facilitate plant immunity against pathogen attack in an ICE1-dependent manner. Cold treatment promoted interactions of NPR1 and TGA3 with ICE1, and increased the ability of the ICE1-TGA3 complex to transcriptionally activate PR1. Together, our results characterize a previously unrecognized role of ICE1 as an indispensable regulatory node linking low temperature activated- and SA-regulated immunity. Discovery of a crucial role of ICE1 in coordinating multiple signals associated with immunity broadens our understanding of plant-pathogen interactions."
Authors: Liangliang Chen and Keiko U. Torii.
Current Biology (2023)
Abstract: "The proper development and function of stomata — turgor-driven valves for efficient gas-exchange and water control — impact plant survival and productivity. It has become apparent that various receptor kinases regulate stomatal development and immunity. Although stomatal development and immunity occur over different cellular time scales, their signaling components and regulatory modules are strikingly similar, and often shared. In this review, we survey the current knowledge of stomatal development and immunity signaling components, and provide a synthesis and perspectives on the key concepts to further understand the conservation and specificity of these two signaling pathways."
Authors: Tabata Rosas-Diaz, Pepe Cana-Quijada, Mengshi Wu, Du Hui, Gemma Fernandez-Barbero, Alberto P. Macho, Roberto Solano, Araceli G. Castillo, Xiao-Wei Wang, Rosa Lozano-Duran and Eduardo R. Bejarano.
Journal of Integrative Pant Biology (2023)
Abstract: "Jasmonates (JAs) are phytohormones that finely regulate critical biological processes, including plant development and defense. JASMONATE ZIM-DOMAIN (JAZ) proteins are crucial transcriptional regulators that keep JA-responsive genes in a repressed state. In the presence of JA-Ile, JAZ repressors are ubiquitinated and targeted for degradation by the ubiquitin/proteasome system, allowing the activation of downstream transcription factors and, consequently, the induction of JA-responsive genes. A growing body of evidence has shown that JA signalling is crucial in defending against plant viruses and their insect vectors. Here, we describe the interaction of C2 proteins from two tomato-infecting geminiviruses from the genus Begomovirus, tomato yellow leaf curl virus (TYLCV) and tomato yellow curl Sardinia virus (TYLCSaV), with the transcriptional repressor JAZ8 from Arabidopsis thaliana and its closest orthologue in tomato, SlJAZ9. Both JAZ and C2 proteins colocalize in the nucleus, forming discrete nuclear speckles. Overexpression of JAZ8 did not lead to altered responses to TYLCV infection in Arabidopsis; however, knock-down of JAZ8 favours geminiviral infection. Low levels of JAZ8 likely affect the viral infection specifically, since JAZ8-silenced plants do not display obvious developmental phenotypes nor present differences in their interaction with the viral insect vector. In summary, our results show that the geminivirus-encoded C2 interacts with JAZ8 in the nucleus, and suggest that this plant protein exerts an anti-geminiviral effect."
Authors: Guojing Shen, Jingxiong Zhang, Yunting Lei, Yuxing Xu and Jianqiang Wu.
Annual Review of Plant Biology (2023)
Abstract: "Parasitic plants use a special organ, the haustorium, to attach to and penetrate host tissues, forming phloem and/or xylem fusion with the host vascular systems. Across this haustorium–host interface, not only water and nutrients are extracted from the host by the parasitic plant, but also secondary metabolites, messenger RNAs, noncoding RNAs, proteins, and systemic signals are transported between the parasite and host and even among different hosts connected by a parasite. Furthermore, mycorrhizal fungi can form common mycelial networks (CMNs) that simultaneously interconnect multiple plants. Increasing lines of evidence suggest that CMNs can function as conduits, transferring stress-related systemic signals between plants. Between-plant signaling mediated by haustoria and CMNs likely has a profound impact on plant interactions with other organisms and adaptation to environmental factors. Here, we summarize the findings regarding between-plant transfer of biomolecules and systemic signals and the current understanding of the physiological and ecological implications of between-plant signaling."
Authors: Shan Li, Pan Wu, Xiaofen Yu, Jinping Cao, Xia Chen, Lei Gao, Kunsong Chen and Donald Grierson.
Cells (2022)
Abstract: "Fleshy fruits are generally hard and unpalatable when unripe; however, as they mature, their quality is transformed by the complex and dynamic genetic and biochemical process of ripening, which affects all cell compartments. Ripening fruits are enriched with nutrients such as acids, sugars, vitamins, attractive volatiles and pigments and develop a pleasant taste and texture and become attractive to eat. Ripening also increases sensitivity to pathogens, and this presents a crucial problem for fruit postharvest transport and storage: how to enhance pathogen resistance while maintaining ripening quality. Fruit development and ripening involve many changes in gene expression regulated by transcription factors (TFs), some of which respond to hormones such as auxin, abscisic acid (ABA) and ethylene. Ethylene response factor (ERF) TFs regulate both fruit ripening and resistance to pathogen stresses. Different ERFs regulate fruit ripening and/or pathogen responses in both fleshy climacteric and non-climacteric fruits and function cooperatively or independently of other TFs. In this review, we summarize the current status of studies on ERFs that regulate fruit ripening and responses to infection by several fungal pathogens, including a systematic ERF transcriptome analysis of fungal grey mould infection of tomato caused by Botrytis cinerea. This deepening understanding of the function of ERFs in fruit ripening and pathogen responses may identify novel approaches for engineering transcriptional regulation to improve fruit quality and pathogen resistance."
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Authors: Yuya Uji, Go Suzuki, Yumi Fujii, Keita Kashihara, Shoko Yamada and Kenji Gomi.
Physiologia Plantarum (2024)
Abstract: "The plant hormone jasmonic acid (JA) is a signalling compound involved in the regulation of cellular defence and development in plants. In this study, we investigated the roles of a JA-responsive MYB transcription factor, JMTF1, in the JA-regulated defence response against rice bacterial blight caused by Xanthomonas oryzae pv. oryzae (Xoo). JMTF1 did not interact with any JASMONATE ZIM-domain (JAZ) proteins. Transgenic rice plants overexpressing JMTF1 showed a JA-hypersensitive phenotype and enhanced resistance against Xoo. JMTF1 upregulated the expression of a peroxidase, OsPrx26, and monoterpene synthase, OsTPS24, which are involved in the biosynthesis of lignin and antibacterial monoterpene, γ-terpinene, respectively. OsPrx26 was mainly expressed in the vascular bundle. Transgenic rice plants overexpressing OsPrx26 showed enhanced resistance against Xoo. In addition to the JA-hypersensitive phenotype, the JMTF1-overexpressing rice plants showed a typical auxin-related phenotype. The leaf divergence and shoot gravitropic responses were defective, and the number of lateral roots decreased significantly in the JMTF1-overexpressing rice plants. JMTF1 downregulated the expression of auxin-responsive genes but upregulated the expression of OsIAA13, a suppressor of auxin signalling. The rice gain-of-function mutant Osiaa13 showed high resistance against Xoo. Transgenic rice plants overexpressing OsEXPA4, a JMTF1-downregulated auxin-responsive gene, showed increased susceptibility to Xoo. JMTF1 is selectively bound to the promoter of OsPrx26 in vivo. These results suggest that JMTF1 positively regulates disease resistance against Xoo by coordinating crosstalk between JA- and auxin-signalling in rice."
Authors: Claus Wasternack and Bettina Hause.
Molecular Plant (2024)
Excerpts: "Ubiquination of JAZs upon binding of JA-Ile to the COI-JAZ complex within the SCFCOI1 E3 ubiquitin ligase complex leads to proteasomal degradation of JAZs and is followed by release of JA-related transcription factors, such as MYC2, the master switch of JA signaling, leading to switch on of JA-induced gene expression (Howe et al., 2018). COI1 is the dominant F-box protein involved in JA perception (Howe et al., 2018). A crucial point was, whether one or more other of the 700 F-box proteins of Arabidopsis are somehow involved in JA signaling. Recently, the F-box protein AT3G44326 was identified to act specifically in B. cinerea-induced resistance by inhibiting the JAO/JOX-mediated JA catabolism (Zhang et al., 2024) (Figure 1). This is the first example, how plant immunity can be increased by suppressing degradation of JA."
"This points to the fact that BFP1 might play a role in regulating JA-mediated defense response in leaves but is not involved in JA-induced growth inhibition. In the same regard, BFP1 over-expression lines showed enhanced expression of PDF1.2 and VSP2 upon JA application but not in the resting state indicating BFP1 as a positive regulator in defense response."
"Summarizing, the paper by Zhang et al. (2024) illustrates nicely the important role of balance of synthesis and degradation of JA and its derivatives in the immune response against various pathogens. The exclusive action of BFP1 as positive regulator of JA-dependent processes in defense without causing fitness costs allows the development of a new strategy of enhancing plant’s disease resistance."
Authors: Andrea Genre, Serena Capitanio and Paola Bonfante.
In Book: Fungal Associations (2024)
Abstract: "Mycorrhizas are mutualistic interactions that the majority of land plants establish with a heterogeneous group of soil fungi; their distribution and diversity have supported the success of plants on the planet. Among all different types of mycorrhizas, arbuscular mycorrhiza (AM) is the most ancient and the most common in host plants of all major crops. The functional core of AM is a finely branched fungal structure called the arbuscule. Arbuscules are hosted inside living root cells, within a specialized cell compartment that is generated through a precise sequence of molecular and cellular events. Over the last 10 years, the application of novel technologies, such as genome sequencing, high-throughput transcriptomics, and live cell imaging, has generated substantial advances in our knowledge of such events. Here, we present a synopsis of the recent literature on the interactions between AM fungi and their hosts, with an evolutionary-developmental focus on the intimate contact that develops between plant cells and fungal hyphae, in terms of molecular signaling, nutrient exchange, and cell organization."
Authors: Jordan Powers, Xing Zhang, Andres V. Reyes, Raul Zavaliev, Shou-Ling Xu and Xinnian Dong.
bioRxiv (2024)
Abstract: "For over 60 years, salicylic acid (SA) has been known as a plant immune signal required for both basal and systemic acquired resistance (SAR). SA activates these immune responses by reprogramming up to 20% of the transcriptome through the function of NPR1. However, components in the NPR1-signaling hub, which appears as nuclear condensates, and the NPR1-signaling cascade remained elusive due to difficulties in studying transcriptional cofactors whose chromatin associations are often indirect and transient. To overcome this challenge, we applied TurboID to divulge the NPR1-proxiome, which detected almost all known NPR1-interactors as well as new components of transcription-related complexes. Testing of new components showed that chromatin remodeling and histone demethylation contribute to SA-induced resistance. Globally, NPR1-proxiome shares a striking similarity to GBPL3-proxiome involved in SA synthesis, except associated transcription factors (TFs), suggesting that common regulatory modules are recruited to reprogram specific transcriptomes by transcriptional cofactors, like NPR1, through binding to unique TFs. Stepwise greenCUT&RUN analyses showed that, upon SA-induction, NPR1 initiates the transcriptional cascade primarily through association with TGA TFs to induce expression of secondary TFs, predominantly WRKYs. WRKY54 and WRKY70 then play a major role in inducing immune-output genes without interacting with NPR1 at the chromatin. Moreover, a loss of NPR1 condensate formation decreases its chromatin-association and transcriptional activity, indicating the importance of condensates in organizing the NPR1-signaling hub and initiating the transcriptional cascade. This study demonstrates how combinatorial applications of TurboID, and stepwise greenCUT&RUN transcend traditional genetic methods to globally map signaling hubs and transcriptional cascades."
Authors: Mikayla Carty, Ruize Zhang, Ziyue Li, Daowen Wang and Zheng Qing Fu.
Molecular Plant (2023)
Excerpts: "Aphids are highly destructive pests that greatly hurt the agricultural industry. Transmitting over 40% of plant viruses, they are the most destructive pests that the agricultural industry faces (Gong et al., 2023). Aphids feed on plants, and in doing so, they consume sap from one plant and then move to another and inject their saliva into the new plant (Hooks and Fereres, 2006). This cycle causes diseases and viral pathogens to become rampant between plants as the aphids carry viral pathogens from one plant to another and so on. In response to this harmful process, plants release volatile organic compounds (VOCs) in order to elicit airborne defense (AD) mechanisms to counterstrike harmful aphids and aphid-transmitted viruses (Hooks and Fereres, 2006). A fascinating recent study published from Yule Liu’s lab revealed that methyl-salicylate (MeSA) serves as a VOC in the AD battle against aphids and viruses (Gong et al., 2023).
"Gong et al. discovered that phloem-feeding insects like aphids trigger a SA response in attacked plants, leading to an increase in SA levels (Gong et al., 2023). This SA increase activates the NAC2 transcription factor, which in turn binds to the SAMT1 promoter and induces the transcription of SAMT1, encoding the enzyme responsible for converting SA into MeSA (Figure 1A). This marks the start of the AD process. MeSA, as a predominant VOC induced by aphid attacks, will then reach the neighboring plants (Gong et al., 2023)."
"In response to this plant adaptation, some aphid-transmitted viruses have evolved mechanisms to suppress MeSA emission in aphid-attacked plants, impairing the induction of plant defenses against virus infection and aphid infestation in nearby plants and therefore effectively fighting against AD. This is accomplished through helicase-domain-containing proteins that interfere with NAC2. For example, CMV1a interacts with NAC2 and promotes NAC2 degradation through the 26S proteasome, disrupting the process that produces AD-inducing MeSA (Figure 1B) (Gong et al., 2023)."
Authors: Shan Liu, Faisal Islam, Jianping Chen, Zongtao Sun and Jian Chen.
Plant Communications (2024)
Excerpts: "Plants have evolved to generate and release a wide array of volatile organic compounds (VOCs) when challenged by environmental stimuli such as biotic and abiotic stresses, which facilitate their reproduction, defense responses, and plant-plant communication (Karban, 2021). Once emitted, some VOCs can elicit defense signaling in neighboring plants by interacting with specific receptor(s), a phenomenon referred to as airborne defense (AD) (Loreto and D’Auria, 2022)."
"MeSA plays important roles in plant AD. However, the mode of action of MeSA bridging interplant communication and inducing plant AD remains unclear. The recent study of Gong et al. (2023) unveiled an integral MeSA-mediated AD signal circuit composed of MeSA, salicylic acid-binding protein-2 (SABP2), the transcription factor NAC2, and salicylic acid-carboxylmethyltransferase-1 (SAMT1). This investigation deciphers the details of the molecular genetic mechanism by which MeSA is generated and perceived by neighboring plants as a plant AD agent (Gong et al., 2023)."
"In the interplay of aphid-plant-virus, aphid attack induces a high level of SA in plants, which activates NAC2-modulated SAMT1 transcription, thus upregulating biosynthesis and volatilization of MeSA, and conferring plant SAR against viruses (Figure 1A). As an airborne signal, volatile MeSA disperses and is then perceived by neighboring plants through the odorant-binding protein-like receptor SABP2, which converts MeSA into SA, leading to NAC2–SAMT1 activation to produce more MeSA against aphid infestation (Figure 1A). To counteract plant AD, CMV deploys a helicase domain-containing protein, possibly a conserved tactic among multiple virus species, to relocate and degrade NAC2 and thus promote aphid survival and virus infection by undermining the MeSA–SABP2–NAC2–SAMT1 signaling cascade (Figure 1B).
Authors: Mikayla Carty, Chen Wang, Daowen Wang and Zheng Qing Fu.
Trends in Parasitology (2023)
Abstract: "Plant-parasitic nematodes (PPNs) pose a serious threat to world crop production and global food security. However, our understanding of the molecular mechanisms underlying plant defense against PPNs remains very limited. Recently, Zou et al. reported that the interplay between autophagy and jasmonate pathways mediates plant immunity against root-knot nematodes."
Authors: Keming Yang, Ruixin Fu, Haichao Feng, Gaofei Jiang, Omri Finkel, Tianyu Sun, Mingchun Liu, Baowen Huang, Shan Li, Xiaofang Wang, Tianjie Yang, Yikui Wang, Shimei Wang, Yangchun Xu, Qirong Shen, Ville-Petri Friman, Alexandre Jousset and Zhong Wei.
Molecular Plant (2023)
Abstract: "The RIPENING-INHIBITOR (RIN) transcriptional factor is a key regulator governing fruit ripening. While RIN also affects other physiological processes, its potential roles in triggering interactions with the rhizosphere microbiome and plant health are unknown. Here we show that RIN affects microbiome-mediated disease resistance via root exudation, leading to recruitment of microbiota that suppress the soil-borne, phytopathogenic Ralstonia solanacearum bacterium. Compared with the wild-type (WT) plant, RIN mutants had different root exudate profiles, which were associated with distinct changes in microbiome composition and diversity. Specifically, the relative abundances of antibiosis-associated genes and pathogen-suppressing Actinobacteria (Streptomyces) were clearly lower in the rhizosphere of rin mutants. The composition, diversity, and suppressiveness of rin plant microbiomes could be restored by the application of 3-hydroxyflavone and riboflavin, which were exuded in much lower concentrations by the rin mutant. Interestingly, RIN-mediated effects on root exudates, Actinobacteria, and disease suppression were evident from the seedling stage, indicating that RIN plays a dual role in the early assembly of disease-suppressive microbiota and late fruit development. Collectively, our work suggests that, while plant disease resistance is a complex trait driven by interactions between the plant, rhizosphere microbiome, and the pathogen, it can be indirectly manipulated using “prebiotic” compounds that promote the recruitment of disease-suppressive microbiota."
Authors: Jinping Zou, Xinlin Chen, Chenxu Liu, Mingyue Guo, Mukesh Kumar Kanwar, Zhenyu Qi, Ping Yang, Guanghui Wang, Yan Bao, Diane C. Bassham, Jingquan Yu and Jie Zhou
Nature Communications (2023)
Editor's view: Autophagy plays a critical role in plant immunity. Here the authors show that in tomato, autophagy promotes defense against root-knot nematodes by promoting degradation of negative regulators of jasmonic acid signaling.
Abstract: "Autophagy, as an intracellular degradation system, plays a critical role in plant immunity. However, the involvement of autophagy in the plant immune system and its function in plant nematode resistance are largely unknown. Here, we show that root-knot nematode (RKN; Meloidogyne incognita) infection induces autophagy in tomato (Solanum lycopersicum) and different atg mutants exhibit high sensitivity to RKNs. The jasmonate (JA) signaling negative regulators JASMONATE-ASSOCIATED MYC2-LIKE 1 (JAM1), JAM2 and JAM3 interact with ATG8s via an ATG8-interacting motif (AIM), and JAM1 is degraded by autophagy during RKN infection. JAM1 impairs the formation of a transcriptional activation complex between ETHYLENE RESPONSE FACTOR 1 (ERF1) and MEDIATOR 25 (MED25) and interferes with transcriptional regulation of JA-mediated defense-related genes by ERF1. Furthermore, ERF1 acts in a positive feedback loop and regulates autophagy activity by transcriptionally activating ATG expression in response to RKN infection. Therefore, autophagy promotes JA-mediated defense against RKNs via forming a positive feedback circuit in the degradation of JAMs and transcriptional activation by ERF1."
Authors: Yang-Shuo Dai, Di Liu, Wuxiu Guo, Zhi-Xuan Liu, Xue Zhang, Li-Li Shi, De-Mian Zhou, Ling-Na Wang, Kui Kang, Feng-Zhu Wang, Shan-Shan Zhao, Yi-Fang Tan, Tian Hu, Wu Chen, Peng Li, Qing-Ming Zhou, Long-Yu Yuan, Zhenfei Zhang, Yue-Qin Chen, Wen-Qing Zhang, Juan Li, Lu-Jun Yu and Shi Xiao.
Plant Biotechnology Journal (2023)
Abstract: "Brown planthopper (BPH, Nilaparvata lugens), a highly destructive insect pest, poses a serious threat to rice (Oryza sativa) production worldwide. Jasmonates are key phytohormones that regulate plant defences against BPH; however, the molecular link between jasmonates and BPH responses in rice remains largely unknown. Here, we discovered a Poaceae-specific metabolite, mixed-linkage β-1,3;1,4-d-glucan (MLG), which contributes to jasmonate-mediated BPH resistance. MLG levels in rice significantly increased upon BPH attack. Overexpressing OsCslF6, which encodes a glucan synthase that catalyses MLG biosynthesis, significantly enhanced BPH resistance and cell wall thickness in vascular bundles, whereas knockout of OsCslF6 reduced BPH resistance and vascular wall thickness. OsMYC2, a master transcription factor of jasmonate signalling, directly controlled the upregulation of OsCslF6 in response to BPH feeding. The AT-rich domain of the OsCslF6 promoter varies in rice varieties from different locations and natural variants in this domain were associated with BPH resistance. MLG-derived oligosaccharides bound to the plasma membrane-anchored LECTIN RECEPTOR KINASE1 OsLecRK1 and modulated its activity. Thus, our findings suggest that the OsMYC2-OsCslF6 module regulates pest resistance by modulating MLG production to enhance vascular wall thickness and OsLecRK1-mediated defence signalling during rice-BPH interactions."
Authors: Wenchao Zhao, Jingjing Liang, Huang Huang, Jinshan Yang, Jiaping Feng, Lulu Sun, Rui Yang, Mengjia Zhao, Jianli Wang and Shaohui Wang.
New Phytologist (2023)
Abstract: "JA is involved in the modulation of defence and growth activities in plants. The best-characterized growth-defence trade-offs stem from antagonistic crosstalk among hormones. In this study, we first confirmed that JA negatively regulates root-knot nematode (RKN) susceptibility via the root exudates (REs) of tomato plants. Omics and toxicological analyses implied that kaempferol, a type of flavonol, from REs has a negative effect on RKN infection. We demonstrated that SlMYB57 negatively regulated kaempferol contents in tomato roots, whereas SlMYB108/112 had the opposite effect. We revealed that JA fine-tuned the homeostasis of kaempferol via SlMYB-mediated transcriptional regulation and the interaction between SlJAZs and SlMYBs, thus ensuring a balance between lateral root (LR) development and RKN susceptibility. Overall, this work provides novel insights into JA-modulated LR development and RKN susceptibility mechanisms and elucidates a trade-off model mediated by JA in plants encountering stress."
Authors: Pingyu Wang, Huimin Jia, Ting Guo, Yuanyuan Zhang, Wanqing Wang, Hideki Nishimura, Zhengguo Li and Yoji Kawano.
Journal of Experimental Botany (2023)
Abstract: "Small signaling peptides play important roles in various plant processes, but information regarding their involvement in plant immunity is limited. We previously identified a novel small secreted protein in rice, named immune response peptide 1 (IRP1). Here, we studied IRP1 functions in rice immunity. Rice plants overexpressing IRP1 enhanced resistance to the virulent rice blast fungus. Application of IRP1 peptide to rice suspension cells triggered the expression of IRP1 itself and the defense gene PAL1. RNA-seq results revealed that 84% of genes upregulated by IRP1 peptide were also induced by a microbe-associated molecular pattern(MAMP) chitin, including 13 OsWRKY transcription factors, indicating that IRP1 and chitin share a similar signaling pathway. Co-treatment with chitin and IRP1 elevated the expression level of PAL1 and OsWRKYs in an additive manner. The increased chitin concentration arrested the induction of IRP1 and PAL1 expressions by IRP1, but cannot affect IRP1-triggered MAPK activation. Collectively, our findings indicate that IRP1 functions as a phytocytokine in rice immunity regulating MAPKs and OsWRKYs that could amplify chitin and other signaling pathways, and provide new insights into how MAMPs and phytocytokines cooperatively regulate rice immunity."
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