Plant stomata: a checkpoint of host immunity and pathogen virulence

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Stomata are microscopic pores formed by pairs of guard cells in the epidermis of terrestrial plants; they are essential for gas exchange with the environment and controlling water loss. Accordingly, plants regulate stomatal aperture in response to environmental conditions, such as relative humidity, CO2 concentration, and light intensity. Stomatal openings are also a major route of pathogen entry into the plant and plants have evolved mechanisms to regulate stomatal aperture as an immune response against bacterial invasion. In this review, we highlight studies that begin to elucidate signaling events involved in bacterium-triggered stomatal closure and discuss how pathogens may have exploited environmental conditions or, in some cases, have evolved virulence factors to actively counter stomatal closure to facilitate invasion.

Introduction

The phyllosphere (i.e., aerial parts of terrestrial plants) provides one of the most important niches for microbial inhabitation [1]. Numerous bacteria, including plant and human pathogens, can survive and even proliferate on the plant surface as epiphytes. To initiate pathogenesis, plant pathogenic bacteria must first enter plant tissues. Unlike fungal pathogens, bacteria lack the ability to directly penetrate the plant epidermis; therefore, they rely entirely on natural openings or accidental wounds to enter internal tissues.

The stomate is one such natural opening in the plant epidermis and has long been recognized as a major point of entry for plant pathogenic bacteria [2]. However, until recently stomata have generally been considered to be passive portals of entry for plant pathogenic bacteria. Melotto and colleagues [3] noted that plant stomata close in response to a plant pathogen, Pseudomonas syringae pv. tomato (Pst) DC3000, and a human pathogen, Escherichia coli O157:H7. Interestingly, this response can also be triggered by well-characterized pathogen/microbe-associated molecular patterns (PAMPs or MAMPs; see below), such as flg22 (a peptide derived from bacterial flagellin) and lipopolysaccharide (LPS). This observation suggests that bacterium-triggered stomatal closure is an output of PAMP-triggered immunity [3]. In the past few years, further studies have been published on this topic; we will discuss these in this review.

Section snippets

Role of pattern-recognition receptors (PRRs) in stomatal closure

MAMPs are molecules that are generally conserved among pathogenic and non-pathogenic microbes [4]. Well-defined MAMPs include flg22, elf18 (a peptide derived from elongation factor EF-Tu), LPS, peptidoglycan (PGN) and Ax21 (activator of XA21-mediated immunity) from bacteria; xylanase, chitin, chitosan (a deacylated derivative of chitin) and ergosterol from fungi; and glucan, pep13, and elicitin from oomycetes [5, 6]. Some of these MAMPs were shown to induce stomatal closure in tomato [3],

Signaling cascade involved in pathogen- or MAMP-induced stomatal closure

Studies using purified MAMPs have shown that stomatal closure in response to biotic signals requires the phytohormone abscisic acid (ABA), the guard cell-specific OPEN-STOMATA 1 (OST1) kinase, the production of reactive oxygen species (ROS) and nitric oxide (NO), the heterotrimeric G protein, and the regulation of K+ channels—all of which are hallmarks of abiotic signal-induced stomatal closure ([3, 11•, 14]; Figure 1). These findings suggest that the guard cell signal transductions in response

Pathogen virulence factors involved in countering stomatal closure

Stomatal closure results in reduced pathogen entry into the plant, thereby having a negative impact on pathogenesis. It is not known how different pathogens overcome this host immune response to cause massive infection. As already mentioned, stomata are also regulated by environmental conditions, such as humidity; it is therefore possible that some pathogens may have developed strategies to survive as epiphytes on the plant surface until environmental conditions, such as high humidity, favor

Role of stomate closure in other branches of plant immunity

Recent studies have shown a molecular ‘arms race’ between the plant immune system and pathogen virulence factors. As mentioned above, plants mount MAMP-triggered immunity by recognizing MAMPs/PAMPs. However, MAMP-triggered immunity is often suppressed by virulence effectors produced by pathogens. Plants in turn evolve disease resistance proteins to recognize some of these virulence effectors and activate another branch of immune response known as effector-triggered immunity [28, 29]. Stomatal

Stomatal regulation in plant interaction with human pathogens

In addition to phytopathogenic bacteria, human pathogens are also capable of occupying the phyllosphere, an aspect of the plant–microbe interactions that has major implications for the safety of fresh fruits and vegetables. It is estimated that 76 million cases of food-borne diseases occur yearly in the US (CDC, www.cdc.gov) and there were over 35 major outbreaks in the past decade [30]. The number of serious cases leading to death has been increasing and outbreaks associated with fresh produce

Conclusions

Invasion of plants by microbial pathogens is a critical step in causing plant disease and human pathogen contamination of vegetables, yet our knowledge in this area remains incomplete. As discussed in this review, stomatal entry represents a major route of pathogen invasion and recent studies have begun to shed light on the signal transduction cascades underlying bacterial regulation of stomatal closure and opening. Current results suggest that stomatal closure is a functional output of both

References and recommended reading

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

  • • of special interest

  • •• of outstanding interest

Acknowledgements

We thank Karen Bird for editing and members of the S. Y. H. lab for their comments on the manuscript. We also thank National Institutes of Health (5R01AI068718) and the Chemical Sciences, Geosciences and Biosciences Division, Office of Basic Energy Sciences, Office of Science, U.S. Department of Energy (DE-FG02-91ER20021) for funding support.

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