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Authors: André Kessler and Michael B. Mueller.
Plant Signaling & Behavior (2024)
Abstract: "Plant induced responses to environmental stressors are increasingly studied in a behavioral ecology context. This is particularly true for plant induced responses to herbivory that mediate direct and indirect defenses, and tolerance. These seemingly adaptive alterations of plant defense phenotypes in the context of other environmental conditions have led to the discussion of such responses as intelligent behavior. Here we consider the concept of plant intelligence and some of its predictions for chemical information transfer in plant interaction with other organisms. Within this framework, the flow, perception, integration, and storage of environmental information are considered tunable dials that allow plants to respond adaptively to attacking herbivores while integrating past experiences and environmental cues that are predictive of future conditions. The predictive value of environmental information and the costs of acting on false information are important drivers of the evolution of plant responses to herbivory. We identify integrative priming of defense responses as a mechanism that allows plants to mitigate potential costs associated with acting on false information. The priming mechanisms provide short- and long-term memory that facilitates the integration of environmental cues without imposing significant costs. Finally, we discuss the ecological and evolutionary prediction of the plant intelligence hypothesis."
Authors: Xiaofang Li, Xin Zheng, Nikita Yadav, Shouvik Saha, El-Sayed Salama, Xiangkai Li, Likun Wang and Byong-Hun Jeon.
Plant Communications (2024)
Abstract: The Green Revolution of the mid-20th century transformed agriculture worldwide and has resulted in environmental challenges. A new approach, the Second Green Revolution, seeks to enhance agricultural productivity while minimizing negative environmental impacts. Plant microbiomes play critical roles in plant growth and stress responses, and understanding plant–microbiome interactions is essential for developing sustainable agricultural practices that meet food security and safety challenges, which are among the United Nations Sustainable Development Goals. This review provides a comprehensive exploration of key deterministic processes crucial for developing microbiome management strategies, including the host effect, the facilitator effect, and microbe–microbe interactions. A hierarchical framework for plant microbiome modulation is proposed to bridge the gap between basic research and agricultural applications. This framework emphasizes three levels of modulation: single-strain, synthetic community, and in situ microbiome modulation. Overall, rational management of plant microbiomes has wide-ranging applications in agriculture and can potentially be a core technology for the Second Green Revolution."
Authors: Saumya Jaiswal, Durgesh Kumar Tripathi, Ravi Gupta, Jing He, Zhong-Hua Chen and Vijay Pratap Singh.
Journal of Integrative Plant Biology (2024)
Editor's view: After being infested by aphids, plants trigger a signaling pathway that involves methyl salicylate as an airborne signaling molecule. Thus, the regulation of communication for systemically acquired resistance produced via methyl salicylate is helpful in generating stress resistance among plants against aphid infestation.
Excerpts: "In this commentary, we discuss the signaling role of methyl-salicylate (MeSA) under attack by members of Aphidoidea in plants, which brings about systemically acquired resistance in the aphid-infested plant as well as neighboring plants by acting as a long-distance signaling molecule."
"On the other hand, elevated salicylic acid levels activate the Nicotiana benthamiana transcription factor 2 (NAC2), which gets attached to the promotor region of SAMT1 to activate its transcription process, resulting in conversion of salicylic acid into MeSA. MeSA is transferred via phloem to other plant parts or received by neighboring plants through some specific receptor-like salicylic acid binding protein 2 (SABP2), which also regulates the reconversion of MeSA into salicylic acid to generate specific response against pathogens and insects (Chen et al., 2020; Gong et al., 2023)."
"Although plants are proficient in responding to various environmental cues, MeSA is reported as the key player for interactions among neighboring plants as it is highly aquaphobic and volatile, more so than salicylic acid, along with generating the systemically adapted resilience in plants affected with aphids (Gong et al., 2023). Being a VOC, MeSA can be transferred aerially to neighboring plants in a species-specific manner to produce airborne defense (Gondor et al., 2022)."
Authors; Kohji Yamada and Akira Mine.
Science Advances (2024)
One-sentence summary: In plants, the types and amplitudes of defense outputs against bacterial and fungal pathogens depend on cellular sugars.
Abstract: "Pathogen recognition triggers energy-intensive defense systems. Although successful defense should depend on energy availability, how metabolic information is communicated to defense remains unclear. We show that sugar, especially glucose-6-phosphate (G6P), is critical in coordinating defense in Arabidopsis. Under sugar-sufficient conditions, phosphorylation levels of calcium-dependent protein kinase 5 (CPK5) are elevated by G6P-mediated suppression of protein phosphatases, enhancing defense responses before pathogen invasion. Subsequently, recognition of bacterial flagellin activates sugar transporters, leading to increased cellular G6P, which elicits CPK5-independent signaling promoting synthesis of the phytohormone salicylic acid (SA) for antibacterial defense. In contrast, while perception of fungal chitin does not promote sugar influx or SA accumulation, chitin-induced synthesis of the antifungal compound camalexin requires basal sugar influx activity. By monitoring sugar levels, plants determine defense levels and execute appropriate outputs against bacterial and fungal pathogens. Together, our findings provide a comprehensive view of the roles of sugar in defense."
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: 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, Xiaomeng Zhang, Jianjun Zhao, Yule Liu and Yiguo Hong.
Trends in Plant Science (2024)
Abstract: "Plants emit volatiles as signals to trigger broad physiological responses, including airborne defense (AD). Gong et al. (Nature 2023; 622: 139–145) recently reported the genetic framework of how plants use AD to combat aphids and viruses. The study elucidates the mutualistic relationships between aphids and the viruses they transmit, revealing the broad biological and ecological significance of AD."
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: Siyu Song, Zayda Morales Moreira, Annika L. Briggs, Xue-Cheng Zhang, Andrew C. Diener and Cara H. Haney.
Nature Plants (2023)
One-sentence summary: To avoid autoimmunity against the microbiome, plants use PHYTOSULFOKINE RECEPTOR 1-mediated regulation of salicylic acid signalling to tune the plant growth–defence balance in response to microbiota.
Abstract: "Microbiota benefit their hosts by improving nutrient uptake and pathogen protection. How host immunity restricts microbiota while avoiding autoimmunity is poorly understood. Here we show that the Arabidopsis phytosulfokine receptor 1 (pskr1) mutant displays autoimmunity (plant stunting, defence-gene expression and reduced rhizosphere bacterial growth) in response to growth-promoting Pseudomonas fluorescens. Microbiome profiling and microbiota colonization showed that PSKR1-mediated reduction in bacterial growth and stunting is largely specific to Pseudomonas. Transcriptional profiling demonstrated that PSKR1 regulates the growth–defence trade-off during Pseudomonas colonization: PSKR1 upregulates plant photosynthesis and root growth but suppresses salicylic-acid-mediated defences. Genetic epistasis experiments showed that pskr1 stunting and restriction of bacterial growth are salicylic acid dependent. Finally, we showed that Pseudomonas, but not other bacteria, induces PSKR1 expression in roots, suggesting that Pseudomonas might manipulate plant signalling to promote its colonization. Our data demonstrate a genetic mechanism to coordinate beneficial functions of the microbiome while preventing autoimmunity.
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: Zhicheng Wang, Chenglin Su, Wenyun Hu, Qiao Su and Yushi Luan
Planta (2023)
Main conclusion: Phytophthora infestans effectors manipulate the antagonism of host hormones to interfere with the immune response of plants at different infection stages.
Abstract: "Phytophthora infestans (P. infestans) poses a serious threat to global crop production, and its effectors play an indispensable role in its pathogenicity. However, the function of these effectors during the switch from biotrophy to necrotrophy of P. infestans remains unclear. Further research on the effectors that manipulate the antagonistic response of host hormones is also lacking. In this study, a coexpression analysis and infection assays were performed to identify distinct gene expression changes in both P. infestans and tomato. During the switch from biotrophy to necrotrophy, P. infestans secretes three types of effectors to interfere with host salicylic acid (SA), jasmonic acid (JA), ethylene (ET), and abscisic acid (ABA) levels. The three aforementioned effectors also regulate the host gene expression including NPR1, TGA2.1, PDF1.2, NDR1, ERF3, NCED6, GAI4, which are involved in hormone crosstalk. The changes in plant hormones are mediated by the three types of effectors, which may accelerate infection and drive completion of the P. infestans lifecycle. Our findings provide new insight into plant‒pathogen interactions that may contribute to the prevention growth of hemibiotrophic pathogens."
Authors: Zhe Li and Golam Jalal Ahammed.
Journal of Plant Physiology (2023)
Highlights • eCO2 affects various aspects of plant and pathogen biology directly or indirectly • eCO2 suppresses (hemi)biotrophic pathogens but stimulates necrotrophic pathogens • Phytohormone salicylate (SA) and jasmonate (JA) mediate plant defense at eCO2 • eCO2 promotes SA signaling and represses the JA pathway • eCO2 modulates antagonism between SA and JA and affects plant immunity
Abstract: "Plants respond to elevated CO2 (eCO2) via a variety of signaling pathways that often rely on plant hormones. In particular, phytohormone salicylic acid (SA) and jasmonic acid (JA) play a key role in plant defense against diverse pathogens at eCO2. eCO2 affects the synthesis and signaling of SA and/or JA and variations in SA and JA signaling lead to variations in plant defense responses to pathogens. In general, eCO2 promotes SA signaling and represses the JA pathway, and thus diseases caused by biotrophic and hemibiotrophic pathogens are typically suppressed, while the incidence and severity of diseases caused by necrotrophic fungal pathogens are enhanced under eCO2 conditions. Moreover, eCO2-induced modulation of antagonism between SA and JA leads to altered plant immunity to different pathogens. Notably, research in this area has often yielded contradictory findings and these responses vary depending on plant species, growth conditions, photoperiod, and fertilizer management. In this review, we focus on the recent advances in SA, and JA signaling pathways in plant defense and their involvement in plant immune responses to pathogens under eCO2. Since atmospheric CO2 will continue to increase, it is crucial to further explore how eCO2 may alter plant defense and host-pathogen interactions in the context of climate change in both natural as well as agricultural ecosystems."
Authors: Xianbi Li, Guoqing Niu, Yanhua Fan, Wenying Liu, Qian Wu, Chen Yu, Jian Wang, Yuehua Xiao, Lei Hou, Dan Jin, Song Chen, Rongyu Hu, Yumei Yang and Yan Pei.
Plant Communications (2023)
Abstract: "In plant immunity, salicylic acid (SA) and jasmonic acid (JA), two mutually antagonistic hormones, are implicated in resistance to biotrophic and necrotrophic pathogens, respectively. To engineer plants with enhanced resistance against a broad-spectrum of pathogens, promoters that can respond to both SA and JA signals are desperately required. However, few natural pathogen-inducible promoters are available for this purpose. To remedy this problem, we herein provide a strategy to synthesize dual SA and JA-responsive promoters by combining SA- and JA-responsive cis-elements based on the interaction between their cognate trans-acting factors. The resulting promoters can respond quickly and strongly to both SA and MeJA, or encountered with different types of phytopathogens. Using a synthetic promoter to control the expression of an antimicrobial peptide, transgenic plants displayed enhanced resistance against a diverse range of phytopathogens, encompassing biotrophic, necrotrophic, and hemibiotrophic pathogens. Inspired by this, a dual-inducible promoter responsive to antagonistic auxin and cytokinin was generated in a similar manner, indicating our strategy can be utilized for the design of other biotic- or abiotic-inducible systems."
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Authors: Tingliang Xu, Xiaowen Zheng, Yi Yang, Shumin Yang, Xingwan Yi, Chao Yu, Le Luo, Jia Wang, Tangren Cheng, Qixiang Zhang and Huitang Pan.
Planta (2024)
Main conclusion: IAA cooperates with JA to inhibit SA and negatively regulates rose black spot disease resistance.
Abstract: "Black spot disease caused by the fungus Marssonina rosae is the most prevalent and severe ailment in rose cultivation, leading to the appearance of black spots on leaves and eventual leaf fall, significantly impacting the utilization of roses in gardens. Salicylic acid (SA) and jasmonic acid (JA) are pivotal hormones that collaborate with indole-3 acetic acid (IAA) in regulating plant defense responses; however, the detailed mechanisms underlying the induction of black spot disease resistance by IAA, JA, and SA remain unclear. In this study, transcript analysis was conducted on resistant (R13–54) and susceptible (R12–26) lines following M. rosae infection. In addition, the impact of exogenous interference with IAA on SA- and JA-mediated disease resistance was examined. The continuous accumulation of JA, in synergy with IAA, inhibited activation of the SA signaling pathway in the early infection stage, thereby negatively regulating the induction of effective resistance to black spot disease. IAA administration alleviated the inhibition of SA on JA to negatively regulate the resistance of susceptible strains by further enhancing the synthesis and accumulation of JA. However, IAA did not contribute to the negative regulation of black spot resistance when high levels of JA were inhibited. Virus-induced gene silencing of RcTIFY10A, an inhibitor of the JA signaling pathway, further suggested that IAA upregulation led to a decrease in disease resistance, a phenomenon not observed when the JA signal was inhibited. Collectively, these findings indicate that the IAA-mediated negative regulation of black spot disease resistance relies on activation of the JA signaling pathway."
Authors: Dacheng Wang, Lirong Wei, Jinbiao Ma, Kenichi Tsuda, Chunhao Jiang and Yiming Wang.
Cell Reports (2024)
Editor's view: The plant microbiome helps to shape the immune system to counter infection of pathogens. Wang et al. show that the root-associated Bacillus cereus NJ01 significantly enhances plant resistance. The EDS1-WRKY18 module is required for NJ01-enhanced disease resistance through activation of SA- and ABA-mediated immunity.
Highlights: • Rhizobacterium Bacillus cereus NJ01 enhances plant resistance against bacterial pathogens • EDS1 enhances WRKY18 DNA-binding activity for the NJ01-enhanced disease resistance • ICS1 and NCED3/5 are downstream of EDS1-WRKY18 for NJ01-enhanced disease resistance
Abstract: "Emerging evidence suggests a beneficial role of rhizobacteria in ameliorating plant disease resistance in an environment-friendly way. In this study, we characterize a rhizobacterium, Bacillus cereus NJ01, that enhances bacterial pathogen resistance in rice and Arabidopsis. Transcriptome analyses show that root inoculation of NJ01 induces the expression of salicylic acid (SA)- and abscisic acid (ABA)-related genes in Arabidopsis leaves. Genetic evidence showed that EDS1, PAD4, and WRKY18 are required for B. cereus NJ01-induced bacterial resistance. An EDS1-PAD4 complex interacts with WRKY18 and enhances its DNA binding activity. WRKY18 directly binds to the W box in the promoter region of the SA biosynthesis gene ICS1 and ABA biosynthesis genes NCED3 and NCED5 and contributes to the NJ01-induced bacterial resistance. Taken together, our findings indicate a role of the EDS1/PAD4-WRKY18 complex in rhizobacteria-induced disease resistance."
Authors: Shai Morin, Peter W. Atkinson and Linda L. Walling.
Annual Review of Entomology (2024)
Abstract: "The rapid advances in available transcriptomic and genomic data and our understanding of the physiology and biochemistry of whitefly–plant interactions have allowed us to gain new and significant insights into the biology of whiteflies and their successful adaptation to host plants. In this review, we provide a comprehensive overview of the mechanisms that whiteflies have evolved to overcome the challenges of feeding on phloem sap. We also highlight the evolution and functions of gene families involved in host perception, evaluation, and manipulation; primary metabolism; and metabolite detoxification. We discuss the emerging themes in plant immunity to whiteflies, focusing on whitefly effectors and their sites of action in plant defense–signaling pathways. We conclude with a discussion of advances in the genetic manipulation of whiteflies and the potential that they hold for exploring the interactions between whiteflies and their host plants, as well as the development of novel strategies for the genetic control of whiteflies."
Authors: Yuli Du, Heng Zhang, Kunpeng Jia, Zongyan Chu, Shican Xu, Lam-Son Phan Tran, Jinggong Guo, Weiqiang Li and Kun Li.
Physiologia Plantarum (2024)
Abstract: "In terrestrial plants, stomata in the leaf epidermis formed by guard cells are the major pathways for gas exchange. However, opened stomata also provide a major channel for pathogen entry. At the pre-invasive stage, plants actively close stomata to prevent pathogen attack, which is termed stomatal immunity, and plant hormones are involved in this process. Here, we summarize recent advances in the role of abscisic acid (ABA) in promoting stomatal immunity to prevent pathogen entry. Additionally, salicylic acid shares common downstream elements with ABA to promote stomatal immunity, whereas reactive oxygen species and Ca2+ act as critical signals to cross-talk with ABA signalling to regulate stomatal movement, and they also enhance the effect of ABA in stomatal immunity. On the other hand, at the post-invasive stage, closed stomata create a water-soaked environment that allows pathogen multiplication, and ABA signalling is hijacked by pathogens to reduce stomatal aperture. Here, we propose a model of dual roles of ABA-mediated stomatal closure during plant-pathogen interaction and offer emerging consequences and questions for ABA-mediated stomatal immunity."
Authors: Steven H. Spoel and Xinnian Dong.
The Plant Cell (2024)
Abstract: "As the most widely used herbal medicine in human history and a major defense hormone in plants against a broad spectrum of pathogens and abiotic stresses, salicylic acid (SA) has attracted major research interest. With applications of modern technologies over the past 30 years, studies of the effects of SA on plant growth, development, and defense have revealed many new research frontiers, and continue to deliver surprises. In this review, we provide an update on recent advances in our understanding of SA metabolism, perception, and signal transduction mechanisms in plant immunity. An overarching theme emerges that SA executes its many functions through intricate regulation at multiple steps: SA biosynthesis is regulated both locally and systemically, while its perception occurs through multiple cellular targets, including metabolic enzymes, redox regulators, transcription cofactors, and most recently, an RNA-binding protein. Moreover, SA orchestrates a complex series of posttranslational modifications of downstream signaling components and promotes the formation of biomolecular condensates that function as cellular signaling hubs. SA also impacts wider cellular functions through crosstalk with other plant hormones. Looking into the future, we propose new areas for exploration on SA functions, which will undoubtedly uncover more surprises for many years to come."
Authors: Muhammad Arslan Mahmood, Muhammad Jawad Akbar Awan, Rubab Zahra Naqvi and Shahid Mansoor.
Trends in Plant Science (2024)
Abstract: "Stressed plants emit a variety of chemicals into the environment, leading to increased pest resistance in neighbouring plants but the genetic and molecular mechanisms of the emissions remain obscure. Recently, Gong et al. identified novel methyl salicylate (MeSA)-mediated airborne defence that confers resistance to neighbouring plants against aphids and viruses."
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: Lingya Yao, Zeyu Jiang, Yiping Wang, Yezhou Hu, Guodong Hao, Weili Zhong, Shiwei Wan and Xiu-Fang Xin.
The EMBO Journal (2023)
Synopsis: Many plant diseases are more severe when air humidity is high; however, the effect of air humidity on host plant biology remains obscure. This report shows that, in very humid conditions, key salicylic acid-mediated plant defenses are suppressed, making plants more vulnerable to infection. High humidity triggers a range of plant physiological responses. Investigating the effects of high humidity on individual plant immune pathways revealed a significant suppression of salicylic acid (SA) accumulation and signaling. Cellular ubiquitination pathways are suppressed in high humidity, including the ubiquitination and activity of the SA receptor NPR1.
Abstract: "The occurrence of plant disease is determined by interactions among host, pathogen, and environment. Air humidity shapes various aspects of plant physiology and high humidity has long been known to promote numerous phyllosphere diseases. However, the molecular basis of how high humidity interferes with plant immunity to favor disease has remained elusive. Here we show that high humidity is associated with an “immuno-compromised” status in Arabidopsis plants. Furthermore, accumulation and signaling of salicylic acid (SA), an important defense hormone, are significantly inhibited under high humidity. NPR1, an SA receptor and central transcriptional co-activator of SA-responsive genes, is less ubiquitinated and displays a lower promoter binding affinity under high humidity. The cellular ubiquitination machinery, particularly the Cullin 3-based E3 ubiquitin ligase mediating NPR1 protein ubiquitination, is downregulated under high humidity. Importantly, under low humidity the Cullin 3a/b mutant plants phenocopy the low SA gene expression and disease susceptibility that is normally observed under high humidity. Our study uncovers a mechanism by which high humidity dampens a major plant defense pathway and provides new insights into the long-observed air humidity influence on diseases."
Authors: Kaitlyn N. Greenwood, Courtney L. King, Isabella Melena, Katherine A. Stegemann, Maura Donnelly, Anna Childers, Raegan Mozal, Carina A. Collins and Benjamin J. Spears.
Plant Direct (2023)
Abstract: "Phloem is a critical tissue for transport of photosynthates and extracellular signals in vascular plants. However, it also represents an ideal environment for pathogens seeking access to valuable host nutrients. Although many vascular pathogens induce economically relevant crop damage, there is still little known about the mechanisms by which immune signaling operates through the phloem. An existing phosphoproteomic dataset was mined to identify proteins that were both phosphorylated in response to the defense-elicitor flagellin (flg22) and expressed in vascular cells. A single candidate, OCTOPUS (OPS), is polarly associated with the plasma membrane of sieve element cells and has been characterized as an inhibitor of brassinosteroid insensitive-2 in promotion of brassinosteroid-related phytohormone signaling. The observation that OPS is differentially phosphorylated in response to flg22 led us to the examine whether OPS may also regulate flg22-induced immune signaling. Two independent alleles of ops exhibited enhanced immunity outputs across multiple signaling branches of PAMP-triggered immunity (PTI), constitutively and in response to flg22 treatment. Together with our observation that interactions between OPS and brassinosteroid insensitive-2 were disrupted by induction of salicylic acid and depletion of brassinosteroid, these data support a model whereby OPS modulates brassinolide and immune signaling to control downstream responses. We present OPS as a novel addition to the list of proteins with documented roles in PAMP-PTI signaling. These results further indicate that immune signaling in the phloem may be a significant and unique component of the host detection and response to pathogens in vascular plants."
Authors: Pei-Cheng Huang, Morgan Tate, Katherine M. Berg-Falloure, Shawn A. Christensen, Jinglan Zhang, Jan Schirawski, Robert Meeley and Michael V. Kolomiets.
Molecular Plant Pathology (2023)
Editor's view: ZmOPR2 functions as a key component of salicylic acid-mediated defences via suppressing jasmonic acid biosynthesis during pathogen infection, leading to its contrasting contribution to either resistance or susceptibility depending on pathogen lifestyle.
Abstract: "Peroxisome-localized oxo-phytodienoic acid (OPDA) reductases (OPR) are enzymes converting 12-OPDA into jasmonic acid (JA). However, the biochemical and physiological functions of the cytoplasmic non-JA producing OPRs remain largely unknown. Here, we generated Mutator-insertional mutants of the maize OPR2 gene and tested its role in resistance to pathogens with distinct lifestyles. Functional analyses showed that the opr2 mutants were more susceptible to the (hemi)biotrophic pathogens Colletotrichum graminicola and Ustilago maydis, but were more resistant to the necrotrophic fungus Cochliobolus heterostrophus. Hormone profiling revealed that increased susceptibility to C. graminicola was associated with decreased salicylic acid (SA) but increased JA levels. Mutation of the JA-producing lipoxygenase 10 (LOX10) reversed this phenotype in the opr2 mutant background, corroborating the notion that JA promotes susceptibility to this pathogen. Exogenous SA did not rescue normal resistance levels in opr2 mutants, suggesting that this SA-inducible gene is the key downstream component of the SA-mediated defences against C. graminicola. Disease assays of the single and double opr2 and lox10 mutants and the JA-deficient opr7opr8 mutants showed that OPR2 negatively regulates JA biosynthesis, and that JA is required for resistance against C. heterostrophus. Overall, this study uncovers a novel function of a non-JA producing OPR as a major negative regulator of JA biosynthesis during pathogen infection, a function that leads to its contrasting contribution to either resistance or susceptibility depending on pathogen lifestyle."
Authors: Abrar Felemban, Juan C. Moreno, Jianing Mi, Shawkat Ali, Arjun Sham, Synan F. AbuQamar and Salim Al-Babili.
bioRxiv (2023)
Abstract: "Carotenoids are isoprenoid pigments vital for photosynthesis. Moreover, they are the precursor of apocarotenoids that include the phytohormones abscisic acid (ABA) and strigolactones (SLs), and retrograde signaling molecules and growth regulators, such as β-cyclocitral and zaxinone. The apocarotenoid β-ionone (β-I) was previously reported to exert antimicrobial effects. Here, we showed that the application of this scent to Arabidopsis plants at micromolar concentrations caused a global reprogramming of gene expression, affecting thousands of transcripts involved in stress tolerance, growth, hormone metabolism, pathogen defense and photosynthesis. These changes, along with modulating the levels of the phytohormones ABA, jasmonic acid and salicylic acid, led to enhanced Arabidopsis resistance to Botrytis cinerea (B.c.), one of the most aggressive and widespread pathogenic fungi affecting numerous plant hosts and causing severe losses of postharvest fruits. Pre-treatment of tobacco and tomato plants with β-I followed by inoculation with B.c. confirms the conserved effect of β-I and induced immune responses in leaves and fruits. Moreover, there was reduced susceptibility to B.c. in LYCOPENE β-CYCLASE- expressing tomato fruits possessing elevated levels of the endogenous β-I, indicating beneficial biological activities of this compound in planta. Our work unraveled β-I as a further carotenoid-derived regulatory metabolite and opens up new possibilities to control B.c. infection by establishing this natural volatile as an environmentally friendly bio-fungicide."
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