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1. Dual Role of Auxin in Regulating Plant Defense and Bacterial Virulence Gene Expression During Pseudomonas syringae PtoDC3000 Pathogenesis

   https://doi.org/10.1094/MPMI-02-20-0047-R  

   Djami-Tchatchou, Arnaud T.; Harrison, Gregory A.; Harper, Chris P.; Wang, Renhou; Prigge, Michael J.; Estelle, Mark; Kunkel, Barbara N. (August 2020, Molecular Plant-Microbe Interactions®)

   null (Ed.)

   Modification of host hormone biology is a common strategy used by plant pathogens to promote disease. For example, the bacterial pathogen strain Pseudomonas syringae DC3000 (PtoDC3000) produces the plant hormone auxin (indole-3-acetic acid [IAA]) to promote PtoDC3000 growth in plant tissue. Previous studies suggest that auxin may promote PtoDC3000 pathogenesis through multiple mechanisms, including both suppression of salicylic acid (SA)-mediated host defenses and via an unknown mechanism that appears to be independent of SA. To test if host auxin signaling is important during pathogenesis, we took advantage of Arabidopsis thaliana lines impaired in either auxin signaling or perception. We found that disruption of auxin signaling in plants expressing an inducible dominant axr2-1 mutation resulted in decreased bacterial growth and that this phenotype was suppressed by introducing the sid2-2 mutation, which impairs SA synthesis. Thus, host auxin signaling is required for normal susceptibility to PtoDC3000 and is involved in suppressing SA-mediated defenses. Unexpectedly, tir1 afb1 afb4 afb5 quadruple-mutant plants lacking four of the six known auxin coreceptors that exhibit decreased auxin perception, supported increased levels of bacterial growth. This mutant exhibited elevated IAA levels and reduced SA-mediated defenses, providing additional evidence that auxin promotes disease by suppressing host defense. We also investigated the hypothesis that IAA promotes PtoDC3000 virulence through a direct effect on the pathogen and found that IAA modulates expression of virulence genes, both in culture and in planta. Thus, in addition to suppressing host defenses, IAA acts as a microbial signaling molecule that regulates bacterial virulence gene expression. 

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2. The Ubiquitin Switch in Plant Stress Response

   https://doi.org/10.3390/plants10020246  

   Doroodian, Paymon; Hua, Zhihua (February 2021, Plants)

   Ubiquitin is a 76 amino acid polypeptide common to all eukaryotic organisms. It functions as a post-translationally modifying mark covalently linked to a large cohort of yet poorly defined protein substrates. The resulting ubiquitylated proteins can rapidly change their activities, cellular localization, or turnover through the 26S proteasome if they are no longer needed or are abnormal. Such a selective modification is essential to many signal transduction pathways particularly in those related to stress responses by rapidly enhancing or quenching output. Hence, this modification system, the so-called ubiquitin-26S proteasome system (UPS), has caught the attention in the plant research community over the last two decades for its roles in plant abiotic and biotic stress responses. Through direct or indirect mediation of plant hormones, the UPS selectively degrades key components in stress signaling to either negatively or positively regulate plant response to a given stimulus. As a result, a tightly regulated signaling network has become of much interest over the years. The ever-increasing changes of the global climate require both the development of new crops to cope with rapid changing environment and new knowledge to survey the dynamics of ecosystem. This review examines how the ubiquitin can switch and tune plant stress response and poses potential avenues to further explore this system. 

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3. Fungal adaptation to plant defences through convergent assembly of metabolic modules

   https://doi.org/10.1111/mec.14943  

   Gluck‐Thaler, Emile; Vijayakumar, Vinod; Slot, Jason C. (December 2018, Molecular Ecology)

   Abstract The ongoing diversification of plant defence compounds exerts dynamic selection pressures on the microorganisms that colonize plant tissues. Evolutionary processes that generate resistance towards these compounds increase microbial fitness by giving access to plant resources and increasing pathogen virulence. These processes entail sequence‐based mechanisms that result in adaptive gene functions, and combinatorial mechanisms that result in novel syntheses of existing gene functions. However, the priority and interactions among these processes in adaptive resistance remain poorly understood. Using a combination of molecular genetic and computational approaches, we investigated the contributions of sequence‐based and combinatorial processes to the evolution of fungal metabolic gene clusters encoding stilbene cleavage oxygenases (SCOs), which catalyse the degradation of biphenolic plant defence compounds known as stilbenes into monophenolic molecules. We present phylogenetic evidence of convergent assembly among three distinct types of SCO gene clusters containing alternate combinations of phenolic catabolism. Multiple evolutionary transitions between different cluster types suggest recurrent selection for distinct gene assemblages. By comparison, we found that the substrate specificities of heterologously expressed SCO enzymes encoded in different clusters types were all limited to stilbenes and related molecules with a 4′‐OH group, and differed modestly in substrate range and activity under the experimental conditions. Together, this work suggests a primary role for genome structural rearrangement, and the importance of enzyme modularity, in promoting fungal metabolic adaptation to plant defence chemistry. 

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4. CONCERTED PLANT GROWTH AND DEFENSE THROUGH TARGETED PHYTOHORMONE CROSSTALK MODIFICATION

   https://doi.org/10.1101/2024.04.08.588615  

   Johnston, Grace A; Berry, Hannah M; Kojima, Mikiko; Sakakibara, Hitoshi; Argueso, Cristiana T (April 2024, bioRxiv)

   ABSTRACT Plant immunity activation often results in suppression of plant growth, particularly in the case of constitutive immune activation. We discovered that signaling of the phytohormone cytokinin (CK), known to regulate plant growth through the control of cell division and shoot apical meristem (SAM) activity, can be suppressed by negative crosstalk with the defense phytohormones jasmonic acid (JA), and most evidently, salicylic acid (SA). We show that changing the negative crosstalk of SA on CK signaling in autoimmunity mutants by targeted increase of endogenous CK levels results in plants resistant to pathogens from diverse lifestyles, and relieves suppression of reproductive growth. Moreover, such changes in crosstalk result in a novel reproductive growth phenotype, suggesting a role for defense phytohormones in the SAM, likely through regulation of nitrogen response and cellular redox status. Our data suggest that targeted phytohormone crosstalk engineering can be used to achieve increased reproductive growth and pathogen resistance. SIGNIFICANCE STATEMENTPlants constantly integrate environmental stimuli with developmental programs to optimize their growth and fitness. Excessive activation of the plant immune system often leads to decreased plant growth, a process known as the growth-defense tradeoff. Here, we adapted phytohormone levels in Arabidopsis reproductive tissues of autoimmunity mutants to change phytohormonal crosstalk and diminish the growth tradeoff, resulting in increased broad resistance to pathogens and decreased growth suppression. Similar approaches to phytohormone crosstalk engineering could be used in different contexts to achieve outcomes of higher plant stress resilience and yield. 

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5. Dynamic genome evolution in a model fern

   https://doi.org/10.1038/s41477-022-01226-7  

   Marchant, D. Blaine; Chen, Guang; Cai, Shengguan; Chen, Fei; Schafran, Peter; Jenkins, Jerry; Shu, Shengqiang; Plott, Chris; Webber, Jenell; Lovell, John T.; et al (September 2022, Nature Plants)

   Abstract The large size and complexity of most fern genomes have hampered efforts to elucidate fundamental aspects of fern biology and land plant evolution through genome-enabled research. Here we present a chromosomal genome assembly and associated methylome, transcriptome and metabolome analyses for the model fern species Ceratopteris richardii . The assembly reveals a history of remarkably dynamic genome evolution including rapid changes in genome content and structure following the most recent whole-genome duplication approximately 60 million years ago. These changes include massive gene loss, rampant tandem duplications and multiple horizontal gene transfers from bacteria, contributing to the diversification of defence-related gene families. The insertion of transposable elements into introns has led to the large size of the Ceratopteris genome and to exceptionally long genes relative to other plants. Gene family analyses indicate that genes directing seed development were co-opted from those controlling the development of fern sporangia, providing insights into seed plant evolution. Our findings and annotated genome assembly extend the utility of Ceratopteris as a model for investigating and teaching plant biology. 

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