Bacterial effectors manipulate plant abscisic acid signaling for creation of an aqueous apoplast

Hu, Yezhou; Ding, Yao; Cai, Boying; Qin, Xiaohui; Wu, Jingni; Yuan, Minhang; Wan, Shiwei; Zhao, Yanping; Xin, Xiu-Fang

doi:10.1016/j.chom.2022.02.002

Cited by 66 publications

(51 citation statements)

References 63 publications

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“…Pst manipulates its host ABA machinery via secretion of its conserved effectors HopM1 and AvrE1 to induce stomatal closure leading to water-soaking (Hu et al, 2022; Roussin-Léveillée et al, 2022). We designed experiments to test whether a deficiency in apoplast hydration was the main reason behind reduced Pst aggressivity under LL.…”

Section: Resultsmentioning

confidence: 99%

“…We designed experiments to test whether a deficiency in apoplast hydration was the main reason behind reduced Pst aggressivity under LL. Since the Arabidopsis aba2-1 mutant was shown to prevent Pst -induced water-soaked lesions (Hu et al, 2022; Roussin-Léveillée et al, 2022), we compared the bacterial levels of these plants infected under LL and LD conditions. We found that, while bacterial population levels were affected in WT plants between LL and LD conditions, they were unaltered in aba2-1 plants (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…A frequent feature of pathogen infection in plants is the creation of an aqueous environment in the plant apoplast, visually noticeable as water-soaked lesions, which is crucial for virulence (Xin et al, 2016). Pst encodes two highly conserved effector proteins, HopM1 and AvrE1, that induce water-soaking lesions (Hu et al, 2022; Roussin-Léveillée et al, 2022; Xin et al, 2016). Notably, these water-soaking effectors stimulate host abscisic acid (ABA) biosynthesis and signaling pathways to induce stomatal closure, resulting in a loss of transpiration and accumulation of water in the apoplast (Hu et al, 2022a; Roussin-Léveillée et al, 2022).…”

Section: Introductionmentioning

confidence: 99%

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Light prevents pathogen-induced aqueous microenvironments via potentiation of salicylic acid signaling

Lajeunesse

Roussin-Léveillée

Boutin

et al. 2022

Preprint

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Upon establishment of an infection, many plant pathogens induce an aqueous microenvironment in the extracellular space of their host, resulting in water-soaked lesions. In the case of Pseudomonas syringae (Pst), this is accomplished through the activity of water-soaking effectors that stimulate abscisic acid (ABA) production and signaling, which results in stomatal closure. This reduces transpiration and induces a microenvironment favorable for bacterial growth. Stomata are also highly sensitive to environmental conditions, including light and circadian rhythm. Here, we show that a period of darkness is required for water-soaking, and that a constant light regime abrogates the water-soaking activity of Pst effectors. Additionally, we show that constant light induces resistance against Pst and that this effect requires salicylic acid (SA). An increase in SA production upon infection under constant light did not affect effector-induced ABA signaling, but rather abrogated ABA's ability to induce stomatal closure. Indeed, under normal diurnal light regimes, application of a SA analog is sufficient to prevent the ability of the pathogen to induce stomatal closure and a water-rich niche in the apoplast. Our results provide a novel approach to interfering with a common virulence strategy, as well as providing a physiological mechanism by which SA functions in defense against certain pathogens.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Light prevents pathogen-induced aqueous microenvironments via potentiation of salicylic acid signaling

Lajeunesse

Roussin-Léveillée

Boutin

et al. 2022

Preprint

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“…P. syringae pv tomato induces water soaking and suppresses SA-dependent responses in A. thaliana using two T3SS effectors HopM1 and AvrE 49 , 50 . Recent work also demonstrated that HopM1 and AvrE induce abscisic acid (ABA) production to close stomata and produce water soaked lesions 51 , 52 . We hypothesized that Xhg may similarly manipulate the immune system, providing protection for S. enterica on tomato leaves.…”

Section: Discussionmentioning

confidence: 99%

Xanthomonas hortorum pv. gardneri TAL effector AvrHah1 is necessary and sufficient for increased persistence of Salmonella enterica on tomato leaves

Cowles

Block

Barak

2022

Sci Rep

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Salmonella enterica is ubiquitous in the plant environment, persisting in the face of UV stress, plant defense responses, desiccation, and nutrient limitation. These fluctuating conditions of the leaf surface result in S. enterica population decline. Biomultipliers, such as the phytopathogenic bacterium Xanthomonas hortorum pv. gardneri (Xhg), alter the phyllosphere to the benefit of S. enterica. Specific Xhg-dependent changes to this niche that promote S. enterica persistence remain unclear, and this work focuses on identifying factors that lead to increased S. enterica survival on leaves. Here, we show that the Xhg transcription activator-like effector AvrHah1 is both necessary and sufficient for increased survival of S. enterica on tomato leaves. An Xhg avrHah1 mutant fails to influence S. enterica survival while addition of avrHah1 to X. vesicatoria provides a gain of function. Our results indicate that although Xhg stimulates a robust immune response from the plant, AvrHah1 is not required for these effects. In addition, we demonstrate that cellular leakage that occurs during disease is independent of AvrHah1. Investigation of the interaction between S. enterica, Xhg, and the plant host provides information regarding how an inhospitable environment changes during infection and can be transformed into a habitable niche.

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“…In Clusters 1 and 2, Gene Ontology (GO) categories related to ABA signaling (“response to abscisic acid, FDR = 0.0025 [Cluster 1] and 0.0073 [Cluster 2],” “response to salt stress, FDR = 0.0023 [Cluster 1] and 0.0025 [Cluster 2] ”, “response to water deprivation, FDR = 0.0031 [Cluster1])” were overrepresented (Figure 2C and Table S4), suggesting that Ct3 specifically induces host ABA responses. ABA promotes plant adaptation to water deficit (Umezawa et al ., 2010), and also influences immunity or susceptibility-related pathways (de Torres-Zabala et al ., 2007; Mine et al ., 2017; Peng et al ., 2019; Huai et al ., 2019; Roussin-Léveillée et al ., 2022; Hu et al ., 2022). qRT-PCR analyses validated increased expression of ABA-responsive plant genes, AtRD29A (Yamaguchi-Shinozaki and Shinozaki, 1993) and AtMAPKKK18 (Okamoto et al ., 2013) during pathogenic Ct3 infection (Figures 2D-E).…”

Section: Resultsmentioning

confidence: 99%

A fungal secondary metabolism gene cluster enables mutualist-pathogen transition in root endophyteColletotrichum tofieldiae

Hiruma

Aoki

Utami

et al. 2022

Preprint

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Plant associated fungi show diverse lifestyles from pathogenic to mutualistic to the host; however, the principles and mechanisms through which they shift the lifestyles require elucidation. The root fungus Colletotrichum tofieldiae (Ct) promotes Arabidopsis thaliana growth under phosphate limiting conditions. We reveal a Ct strain, designated Ct3, that severely inhibits plant growth. Ct3 pathogenesis occurs through activation of host abscisic acid (ABA) pathways via a fungal secondary metabolism gene cluster related to sesquiterpene ABA and botrydial (BOT) biosynthesis. ABA_BOT cluster activation during root infection suppresses host nutrient uptake-related genes and changes the mineral contents, suggesting its role in manipulating host nutrition states. Conversely, disruption or environmental suppression of the cluster renders Ct3 beneficial for plant growth, in a manner dependent on host phosphate starvation response regulators. Our findings indicate that a fungal metabolism cluster provides a means by which infectious fungi modulate lifestyles along the parasitic_mutualistic continuum in fluctuating environments.

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Bacterial effectors manipulate plant abscisic acid signaling for creation of an aqueous apoplast

Cited by 66 publications

References 63 publications

Light prevents pathogen-induced aqueous microenvironments via potentiation of salicylic acid signaling

Light prevents pathogen-induced aqueous microenvironments via potentiation of salicylic acid signaling

Xanthomonas hortorum pv. gardneri TAL effector AvrHah1 is necessary and sufficient for increased persistence of Salmonella enterica on tomato leaves

A fungal secondary metabolism gene cluster enables mutualist-pathogen transition in root endophyteColletotrichum tofieldiae

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