Antagonistic Interaction between Auxin and SA Signaling Pathways Regulates Bacterial Infection through Lateral Root in Arabidopsis

Kong, Xiangpei; Zhang, Chunlei; Zheng, Huizhen; Sun, Min; Zhang, Feng; Zhang, Mengyue; Cui, Fuhao; Lv, Dongping; Liu, Lijing; Guo, Siyi; Zhang, Youming; Yuan, Xian-Zheng; Zhao, Shan; Tian, Huiyu; Ding, Zhaojun

doi:10.1016/j.celrep.2020.108060

Cited by 45 publications

(24 citation statements)

References 64 publications

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“…Pto DC3000 typically colonizes leaf tissue as a pathogenic bacterium. A recent study showed that this bacterium can also colonize plant roots to regulate LR formation and development (Kong et al , 2020), and it cannot develop disease upon root inoculation in a natural soil community (Song et al , 2021). Using the soil‐soak inoculation method, we inoculated A. thaliana seedlings grown under HP and LP conditions with water, Pto DC3000 or B. subtilis strain RIK1285 and used the shoot fresh weight as the alleviated Pi‐starvation phenotypic characteristic.…”

Section: Resultsmentioning

confidence: 99%

“…For example, the fungal pathogen Colletotrichum tofieldiae (Ct) becomes beneficial and transfers phosphorus macronutrients to A. thaliana under Pi‐deficient conditions (Hiruma et al , 2016). Recent studies have shown that Pto DC3000 can also colonize A. thaliana LRs to promote plant growth and fitness (Mang et al , 2017; McClerklin et al , 2018; Kong et al , 2020). As a leaf pathogen, Pto DC3000 might promote Pi absorption in host roots under low‐Pi stress, thus enhancing LR growth.…”

Section: Discussionmentioning

confidence: 99%

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Plant immunity suppression via PHR1‐RALF‐FERONIA shapes the root microbiome to alleviate phosphate starvation

Tang

et al. 2022

The EMBO Journal

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The microbiome plays an important role in shaping plant growth and immunity, but few plant genes and pathways impacting plant microbiome composition have been reported. In Arabidopsis thaliana, the phosphate starvation response (PSR) was recently found to modulate the root microbiome upon phosphate (Pi) starvation through the transcriptional regulator PHR1. Here, we report that A. thaliana PHR1 directly binds to the promoters of rapid alkalinization factor (RALF) genes, and activates their expression under phosphate‐starvation conditions. RALFs in turn suppress complex formation of pathogen‐associated molecular pattern (PAMP)‐triggered immunity (PTI) receptor through FERONIA, a previously‐identified PTI modulator that increases resistance to certain detrimental microorganisms. Suppression of immunity via the PHR1‐RALF‐FERONIA axis allows colonization by specialized root microbiota that help to alleviate phosphate starvation by upregulating the expression of PSR genes. These findings provide a new paradigm for coordination of host‐microbe homeostasis through modulating plant innate immunity after environmental perturbations.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Plant immunity suppression via PHR1‐RALF‐FERONIA shapes the root microbiome to alleviate phosphate starvation

Tang

et al. 2022

The EMBO Journal

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“…Beneficial rhizosphere microorganisms can dramatically affect root development by facilitating root cell division and differentiation (Lopez‐Bucio et al, 2007; Ortiz‐Castro, Martinez‐Trujillo, & Lopez‐Bucio, 2008; Ortiz‐Castro, Valencia‐Cantero, & Lopez‐Bucio, 2008; Patten & Glick, 2002; Zamioudis, Mastranesti, Dhonukshe, Blilou, & Pieterse, 2013; Zou, Li, & Yu, 2010; Zuniga et al, 2013). Pathogenic bacterium can also strongly induce LR formation (Kong et al, 2020). Moreover, a single bacterial genus ( Variovorax ) can manipulate plant hormone levels via metabolic signal interference to maintain root growth in a complex microbiome (Finkel et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

Volatile compounds from beneficial rhizobacteria Bacillus spp. promote periodic lateral root development in Arabidopsis

Shao

Xie

et al. 2021

Plant Cell & Environment

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Lateral root formation is coordinated by both endogenous and external factors. As biotic factors, plant growth-promoting rhizobacteria can affect lateral root formation, while the regulation mechanism is unclear. In this study, by applying various marker lines, we found that volatile compounds (VCs) from Bacillus amyloliquefaciens SQR9 induced higher frequency of DR5 oscillation and prebranch site formation, accelerated the development and emergence of the lateral root primordia and thus promoted lateral root development in Arabidopsis. We demonstrated a critical role of auxin on B. amyloliquefaciens VCs-induced lateral root formation via respective mutants and pharmacological experiments. Our results showed that auxin biosynthesis, polar transport and signalling pathway are involved in B. amyloliquefaciens VCs-induced lateral roots formation. We further showed that acetoin, a major component of B. amyloliquefaciens VCs, is less active in promoting root development compared to VC blends from B. amyloliquefaciens, indicating the presence of yet uncharacterized/unknown VCs might contribute to B. amyloliquefaciens effect on lateral root formation. In summary, our study revealed an auxin-dependent mechanism of B. amyloliquefaciens VCs in regulating lateral root branching in a non-contact manner, and further efforts will explore useful VCs to promote plant root development.

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“…Consistent with bHLH activities (Pireyre and Burow, 2015), combinatorial interactions with TF families regulating SA, auxin, or ABA signaling may contribute to the regulation of diverse biological processes by TCP8 that is reflected in our sequencing data. From the overabundance of auxin-responsive gene candidates identified in our chIP analysis (Figure 1), a role for TCP8 in auxin signaling would be particularly interesting in the context of this study due to known cooperation between auxin and BR and antagonism between auxin and SA that is thought to be exploited by pathogens as a virulence mechanism (McClerklin et al, 2018;Kong et al, 2020).…”

Section: Discussionmentioning

confidence: 99%

The class I TCP transcription factor AtTCP8 is a modulator of phytohormone-responsive signaling networks

Spears

McInturf

Chlebowski

et al. 2021

Preprint

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The plant-specific TEOSINTE BRANCHED1/ CYCLOIDEA/ PROLIFERATING CELL FACTOR (TCP) transcription factor family is most closely associated with regulating plant developmental programs. Recently, TCPs were also shown to mediate host immune signaling, both as targets of pathogen virulence factors and regulators of plant defense genes. However, any comprehensive characterization of TCP gene targets is still lacking. Loss of the class I TCP AtTCP8 attenuates early immune signaling, and when combined with mutations in AtTCP14 and AtTCP15, additional layers of defense signaling in Arabidopsis thaliana. Here we focus on TCP8, the most poorly characterized of the three to date. We use chIP and RNA-sequencing to identify TCP8-bound gene promoters and differentially regulated genes in the tcp8 mutant, data sets that are heavily enriched in signaling components for multiple phytohormone pathways, including brassinosteroids (BRs), auxin, and jasmonic acid (JA). Using BR signaling as a representative example, we show that TCP8 directly binds and activates the promoters of the key BR transcriptional regulators BZR1 and BZR2/BES1. Furthermore, tcp8 mutant seedlings exhibit altered BR-responsive growth patterns and complementary reductions in BZR2 transcript levels, while the expressed protein demonstrates BR-responsive changes in subnuclear localization and transcriptional activity. We conclude that one explanation for the significant targeting of TCP8 alongside other TCP family members by pathogen effectors may lie in its role as a modulator of brassinosteroid and other plant hormone signaling pathways.

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Antagonistic Interaction between Auxin and SA Signaling Pathways Regulates Bacterial Infection through Lateral Root in Arabidopsis

Cited by 45 publications

References 64 publications

Plant immunity suppression via PHR1‐RALF‐FERONIA shapes the root microbiome to alleviate phosphate starvation

Plant immunity suppression via PHR1‐RALF‐FERONIA shapes the root microbiome to alleviate phosphate starvation

Volatile compounds from beneficial rhizobacteria Bacillus spp. promote periodic lateral root development in Arabidopsis

The class I TCP transcription factor AtTCP8 is a modulator of phytohormone-responsive signaling networks

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