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Phytohormone Pathways As Targets of Pathogens to Facilitate Infection

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Phytohormone Pathways As Targets of Pathogens to Facilitate Infection View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Springer - Publisher Connector Plant Mol Biol (2016) 91:713–725 DOI 10.1007/s11103-016-0452-0 Phytohormone pathways as targets of pathogens to facilitate infection 1,2 1,2 Ka-Wai Ma • Wenbo Ma Received: 2 September 2015 / Accepted: 7 February 2016 / Published online: 15 February 2016 Ó The Author(s) 2016. This article is published with open access at Springerlink.com Abstract Plants are constantly threatened by potential Introduction pathogens. In order to optimize the output of defense against pathogens with distinct lifestyles, plants depend on In order to complete an infection cycle, phytopathogens hormonal networks to fine-tune specific responses and need to enter plant tissues through physical barriers, over- regulate growth-defense tradeoffs. To counteract, patho- come defense responses mounted by the plant immune gens have evolved various strategies to disturb hormonal system, obtain nutrients for proliferation, and eventually be homeostasis and facilitate infection. Many pathogens syn- disseminated to a new host. During the co-evolutionary arms thesize plant hormones; more importantly, toxins and race with plants, successful pathogens evolved virulence effectors are produced to manipulate hormonal crosstalk. factors such as toxins and secreted proteins (aka effectors) to Accumulating evidence has shown that pathogens exert modulate plant physiology (Bender et al. 1999; Torto- extensive effects on plant hormone pathways not only to Alalibo et al. 2009; Dou and Zhou 2012; Dangl et al. 2013). defeat immunity, but also modify habitat structure, opti- A prominent and extensively studied example is the type III mize nutrient acquisition, and facilitate pathogen dissemi- secreted effectors, which are injected by Gram negative nation. In this review, we summarize mechanisms by bacterial pathogens directly into plant cells (Deslandes and which a wide array of pathogens gain benefits from Rivas 2012; Feng and Zhou 2012). Eukaryotic filamentous manipulating plant hormone pathways. pathogens including fungi and oomycetes also produce a large number of effectors that can function inside host cells Keywords Plant immunity Á Pathogen effectors Á (Torto-Alalibo et al. 2009; Wawra et al. 2012; Giraldo and Phytohormones Á Pathogenicity Á Virulence Á Bacterial Valent 2013). Over the past decade, substantial efforts have toxins been invested to understand how effectors facilitate patho- gen colonization and disease development. Through these studies, phytohormone pathways have emerged as important virulence targets. Plant hormones are small molecules that affect a broad range of processes during growth and stress responses K.-W. Ma and W. Ma have contributed equally to this manuscript. (Depuydt and Hardtke 2011;Pieterseetal.2012;Vanstraelen and Benkova 2012). By manipulating plant hormonal path- & Ka-Wai Ma ways, pathogens can further benefit through two mechanisms: [email protected] one, they can suppress defense responses regulated by the & Wenbo Ma ‘‘stress’’ hormones in order to accomplish colonization in [email protected] plant tissues; two, they can hijack plant development and 1 Department of Plant Pathology and Microbiology, University nutrient allocation processes regulated by the ‘‘growth’’ hor- of California, Riverside, CA 92521, USA mones to facilitate sustained colonization and dissemination. 2 Center for Plant Cell Biology, University of California, In this review, we classify major plant hormones into Riverside, CA 92521, USA ‘‘stress’’and ‘‘growth’’hormones and discuss the mechanisms 123 714 Plant Mol Biol (2016) 91:713–725 by which microbial pathogens interfere with their accumu- ethylene (ET). Generally speaking, SA plays a key role in lation and/or signaling. Due to space constrains, we will focus defense against pathogens feeding on live tissues, i.e. with on pathogen effectors and toxins that have been demonstrated a biotrophic lifestyle; and JA/ET is critical to defense to directly manipulate hormonal networks in plants as viru- against pathogens feeding on dead tissues, i.e. with a lence strategies to increase pathogen fitness. Examples from a necrotrophic lifestyle (Glazebrook 2005). In addition, JA wide variety of pathogens (viruses, bacteria, fungi, oomycetes alone is prominent in defense against herbivores (Fig. 1). and herbivores) using different infection strategies will be An important concept that has been established over the discussed. years is the antagonism between SA and JA/ET pathways in response to pathogens with a specific lifestyle (Spoel and Dong 2008; Van der Does et al. 2013). However, analysis Plant hormones as key regulators of immunity using a mutant that is defective in SA, JA and ET pathways supported a more synergistic view in that all three hor- Unlike animals that can move and adapt to survive subop- mones contribute positively to defense against various timal conditions, plants are sessile; therefore, the ability to pathogens with one hormone sector makes larger contri- defeat pathogen infection is critical to survival. Threatened butions than others in response to a specific infection style by a large variety of pests and pathogens, plants have (Tsuda et al. 2009). evolved a sophisticated innate immune system (Spoel and Dong 2012). A basal tier of plant immunity is activated by Toxins and effectors targeting salicylic acid conserved molecular signatures called pathogen/microbe- accumulation associated molecular patterns (PAMPs/MAMPs), which can be recognized by receptor-like kinases known as pattern SA is the first plant hormone with a demonstrated role in recognition receptors (PRRs) (Zipfel 2014). Pattern-trig- defense (White 1979) and has since been studied exten- gered immunity (PTI) is associated with a series of physi- sively. Provided the importance of SA in plant defense, ological responses that confer effective, broad-spectrum many pathogens have evolved strategies to target the SA defense against the majority of potential pathogens (Bigeard pathway, either at the level of biosynthesis/accumulation or et al. 2015). Shortly after pathogen perception, extensive downstream signaling (Fig. 1). transcription reprogramming of genes involved in hormonal A main virulence strategy is to suppress SA accumula- signaling occurs (De Vos et al. 2005), suggesting a key tion through the activity of secreted enzymes that metab- regulatory role of hormones in mounting defense responses. olize SA precursors. For example, the biotrophic fungal Major plant hormones that regulate defense responses pathogen Ustilago maydis, which causes maize smut, include salicylic acid (SA), jasmonic acid (JA) and produces a chorismate mutase (Cmu1) during infection. Fig. 1 A diagram showing the crosstalk among SA, JA and ET signaling pathways and their roles in defense against pathogens/herbivores using distinctive infection strategies. Effectors and toxins target SA, JA and ET signaling to suppress plant defense are presented. Virulence factors produced by biotrophs/hemibiotrophs are highlighted in blue, and those produced by necrotrophs are highlighted in red. Chorismate mutase and isochromatases are produced by both biotrophs and necrotrophs and are highlighted in green. Broken lines indicate indirect manipulation processes or unknown mechanisms 123 Plant Mol Biol (2016) 91:713–725 715 Following pathogen perception, SA is produced from also been suggested to affect SA accumulation. For chorismate via the intermediate isochorismate through the example, HopI1 produced by the hemibiotrophic bacterial activity of the isochorismate synthase (ICS) (Wildermuth pathogen Pseudomonas syringae suppresses SA accumu- et al. 2001). Cmu1 converts chorismate to prephenate, lation in chloroplasts. HopI1 directly interacts with the heat potentially lowering the availability of plastid chorismate shock protein Hsp70 and alters chloroplast thylakoid for SA synthesis (Djamei et al. 2011). Indeed, maize structure (Jelenska et al. 2007, 2010). However, how HopI1 infected with a Cmu1 mutant of U. maydis accumulated interferes with SA production remains elusive. more SA and exhibited attenuated disease symptoms compared with plants infected with wild-type strain (Dja- Toxins and effectors targeting salicylic acid mei et al. 2011). Many biotrophic and hemibiotrophic signaling pathogens produce chorismate mutases that can potentially benefit infection (Djamei et al. 2011). Interestingly, the NPR1 (NONEXPRESSOR OF PR GENES 1) is an necrotrophic fungal pathogen Sclerotinia sclerotiorum also essential component in SA-dependent defense. Upon produces a putative chorismate mutase. Pretreatment of the pathogen perception, SA potentiates the reduction of the SA analog benzothiadiazole (BTH) on rapeseed plants oligomeric form of NPR1 in cytoplasm to a monomeric resulted in an approximately 40 % reduction on lesion form through redox changes (Mou et al. 2003). Monomeric sizes caused by S. sclerotiorum, suggesting a positive role NPR1 is then relocated to the nucleus and activates the of SA in defense against S. sclerotiorum (Novakova et al. expression of SA-responsive genes. NPR1-regulated SA 2014). This observation indicates that the putative choris- signaling is tightly regulated through post-translational mate mutase produced by S. sclerotiorum may promote modifications and proteasomal degradation. In particular, infection by reducing SA accumulation. proper turnover of NPR1 is required for the perpetuation of Another secreted enzyme with the ability to suppress
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