Controlling hormone signaling is a plant and pathogen challenge for growth and survival

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Plants and pathogens have continuously confronted each other during evolution in a battle for growth and survival. New advances in the field have provided fascinating insights into the mechanisms that have co-evolved to gain a competitive advantage in this battle. When plants encounter an invading pathogen, not only responses signaled by defense hormones are activated to restrict pathogen invasion, but also the modulation of additional hormone pathways is required to serve other purposes, which are equally important for plant survival, such as re-allocation of resources, control of cell death, regulation of water stress, and modification of plant architecture. Notably, pathogens can counteract both types of responses as a strategy to enhance virulence. Pathogens regulate production and signaling responses of plant hormones during infection, and also produce phytohormones themselves to modulate plant responses. These results indicate that hormone signaling is a relevant component in plant–pathogen interactions, and that the ability to dictate hormonal directionality is critical to the outcome of an interaction.

Introduction

Plants have evolved an immune system to recognize and respond to pathogen attack. In recent years there has been much progress in understanding this plant defense strategy. Numerous components involved in pathogen perception, signal generation and transmission, and activation of defense products restricting pathogen invasion, have been identified. Compelling evidence demonstrates that hormones such as salicylic acid (SA), jasmonates (JAs) and ethylene (ET) are the primary signals inducing defense responses through recognized defense hormone signaling pathways. Significant insight has also been gained into the machinery used by pathogens to invade plant tissues, including their strategies to interfere with the activation of plant defense.

Appropriate re-allocation of limiting resources to energy-costly induced defense responses, as opposed to demands for growth and reproduction, is critical to triggering immunity in plants. Emerging data is starting to unravel the mechanisms used by plants to maintain an equilibrium between these two processes, which is fundamental for their survival and effective competition with other plant species. Recent studies demonstrate that, in addition to known defense pathways (signaled by SA, JAs and ET), oxylipins other than JA, and hormones such as brassinosteroids (BL), auxins, gibberellins (GA), cytokinins (CK), and abscisic acid (ABA), play roles in plant responses to pathogen assault. Upon microbial attack, plants modify the relative abundance of these hormones, and the expression of their responsive genes, as an instrument to activate an efficient defense response allowing plant survival. Importantly, pathogens can counteract this strategy by interfering with these plant hormonal changes and also by producing plant hormones themselves as a component of their invading strategy [1]. Here, we outline the latest discoveries showing the involvement of multiple hormone signaling pathways in plant defense, and report the most striking illustrations of the interaction between distinct pathways and how pathogens interfere with these signaling processes to colonize plants.

Section snippets

Activation of immunity and interactions between defense signaling pathways

Our understanding of the plant immune system has increased enormously in the last decade. A major achievement has been the demonstration that plants use two generalized modes of recognition to sense a harmful microbe. First, perception of conserved microbial molecules (generally designated as microbe associated molecular patterns or MAMPs) by pattern recognition receptors (PRRs) which are generally localized at the cell surface [2, 3, 4]. This initial recognition induces basal resistance or

Plant and pathogen oxylipins modulate defense and susceptibility

JA is an essential hormone for the regulation of defense and developmental responses. It belongs to a family of active molecules, the oxylipins, that originate in the oxidation of various fatty acids usually by the activities of lipoxygenases (9-lipoxygenases and 13-lipoxygenases) and α-dioxygenases. Production of oxylipins and phytoprostanes, a group of non-enzymatically formed oxylipins [20, 21], is a universal response of plants to pathogen attack. Given the importance of the

Changes in growth promoting hormones in plants during pathogen infection

Important growth and developmental processes are executed through signaling pathways governed by hormones such as BL, auxins, CK and GA. In addition, there is increasing evidence that regulation of these signaling pathways helps determine the outcome of a plant–pathogen interaction.

BLs are essential hormones for plant growth and development. Genetic and molecular analyses have defined key components of the BL signaling pathway, including a cell surface leucine repeat-like kinase receptor BRI1,

Modulation of ABA content and signaling during plant–pathogen interactions

A number of recent publications have described altered ABA levels during the interaction of plants with invading pathogens. Distinct actions of this hormone depend upon the infection stage and the specific host pathogen interaction. At a pre-invasion phase, plants enhanced resistance to application of P. syringae pv. tomato DC3000 by inducing stomatal closure and restricting pathogen entry [32]. That the ABA-deficient mutant aba3-1 was more susceptible to P. syringae pv. tomato DC3000 when it

Conclusions and future prospects

Recent studies of plant–pathogen interactions have provided compelling evidence to support the importance of plant hormone signaling in determining the outcome of the interaction. By modulating hormone signaling pathways plants contribute not only directly to defense but also appear to control vital processes for resistance such as distribution of resources between defense and requirements for growth, cell death, water, and plant architecture. Pathogens on the other hand, have evolved invading

References and recommended reading

Papers of particular interest, published within the period of the review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

We thank J Paz-Ares and R Solano for constructive comments and stimulating discussions. This work was supported by Grant BIO2006-08581 from the Ministry of Education and Science to C.C. MAL was supported by fellowship from the Ministry of Education and Science, GB is a Ramón y Cajal fellow supported by the Spanish Ministry of Education and Science, Consejo Superior de Investigaciones Científicas, Madrid, Spain.

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