Chapter Fourteen - NO and Ca2+: Critical Components of Cytosolic Signaling Systems Involved in Stomatal Immune Responses
Introduction
Nitric oxide (NO) is a free radical gas identified as a ubiquitous secondary messenger involved in a plethora of physiological processes in plants, such as seed germination, flowering, pollen tube growth, root growth, stomatal closure, fruit ripening and senescence (Besson-Bard et al., 2008, Simontacchi et al., 2013). In the past two decades, an extensive body of evidence has supported the essential role of NO in plant defense responses to invading pathogens by triggering hypersensitive response (HR) or upregulating defense gene expression (Dangl, 1998, Durner et al., 1998, Jeandroz et al., 2013, Ma, 2011, Ma et al., 2013, Polverari et al., 2003, Romero-Puertas et al., 2004, Trapet et al., 2014, Wendehenne et al., 2001, Zottini et al., 2009). Although NO generation contributing to HR development is due to l-Arginine (L-Arg)-dependent nitric oxide synthase (NOS) activity (Delledonne et al., 1998, Zhang et al., 2003), the exact NO enzymatic biosynthesis pathway is still a controversial topic (Moreau, Lindermayr, Durner, & Klessig, 2010). Nevertheless, the application of a mammalian NOS inhibitors diminishes HR in Arabidopsis and Nicotiana spp. (Delledonne et al., 1998; Huang & Knopp, 1998). Inoculation with an avirulent pathogen elicits an NO burst in Arabidopsis leaf tissue (Zeier et al., 2004, Zhang et al., 2003) and this NO generation is blocked by an NOS inhibitor (Zhang et al., 2003).
Another critical and early component in plant immune signaling cascades is Ca2+, whose cytosolic concentration is transiently elevated causing a Ca2+ burst. The perception of evolutionarily conserved components of microbial invaders known as microbe-associated molecular patterns (MAMPs), such as flagellin, elongation factor-Tu (EF-Tu), lipopolysaccharide (LPS), chitin or damage-associated molecular patterns (DAMP) by plant cells triggers a rapid cytosolic Ca2+ ([Ca2+]cyt) elevation, which is required to activate downstream molecular and physiological processes (Ali et al., 2007, Aslam et al., 2009, Jeworutzki et al., 2010, Kwaaitaal et al., 2011, Ma et al., 2012, Ma et al., 2013). It has been well established that there is a connection between [Ca2+]cyt elevation and NO synthesis during plant innate immune response (Ali et al., 2007, Lamotte et al., 2004, Lecourieux et al., 2006). NO also forms an interaction network with other defense signaling molecules, such as reactive oxygen species (ROS), cyclic nucleotides, mitogen-activated protein kinases (MAPKs; MPK is used when describing specific genes) and phosphatidic acid, to regulate the defense responses in plant cells (Gaupels, Kuruthukulangarakoola, & Durner, 2011). Thus, NO may play a role in immune signaling upstream from the Ca2+ burst in post-translational modification (PTM) of signaling proteins, and also may be involved in the immune cascade downstream from the Ca2+ burst which leads to NO generation.
Stomata are minute pores formed by a pair of guard cells located at the leaf epidermis. They function like ‘mouths’ in plants for regulating gas exchange and transpiratory water loss between the exterior environment and leaf surface. Additionally, stomata act as gateways for the entry of pathogens. The entry of some pathogenic microbes into the plant interior is controlled by stomata movement. Stomatal opening and closing occurs through turgor pressure changes in the pairs of guard cells forming the stomatal pore. Changes in guard cell turgor pressure can be regulated by the plant hormone abscisic acid (ABA) and cytosolic secondary messengers such as NO (García-Mata and Lamattina, 2013, Gayatri et al., 2013, Hancock et al., 2011, Yoshioka et al., 2011).
This chapter discusses and updates knowledge on recent findings of the interdependent relationship of NO and Ca2+ generation and how these signaling molecules contribute to stomatal innate immune responses to pathogens and danger signals.
Section snippets
NO and Ca2+ Involve in Plant Innate Immunity
Plant defense to biotic stress is considered to be initiated by the recognition of exogenous MAMPs or endogenous DAMPs by plasma membrane localized receptors (Gómez-Gómez and Boller, 2000, Gómez-Gómez et al., 1999, Miya et al., 2007, Yamaguchi et al., 2010, Yamaguchi et al., 2006, Zipfel et al., 2006). LPS is an MAMP derived from the outer membrane of Gram-negative bacteria that activates plant cell defenses; however its plant receptor is still unrevealed. It has been generally accepted that [Ca
NO and Ca2+ Signaling in Stomatal Innate Immunity
Stomata are generally the entry port for bacteria invasion. Other phyllosphere microbes, such as fungi and oomycetes can also disrupt stomatal movement during infection. In order to fight the invaders at the first line of defense, guard cells actively regulate their own movement to shut the gate for the strangers (Melotto, Underwood, Koczan, Nomura, & He, 2006). Guard cells restrict pathogen entry by either closing the stomata pore or inhibiting the opening caused by virulence factors, such as
Concluding Perspectives
As a secondary messenger, NO is not studied as extensively as ROS or Ca2+. This is mainly due to the lack of information on the enzymatic synthesis pathway of NO in plant cells that are undergoing signaling cascades involving NO elevation. This is the case with NO production demonstrated in guard cells challenged with elicitors and pathogens. Although most of the studies were conducted using pharmacological compounds, mutants with NO depletion phenotype were generated (Hao et al., 2010,
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