Gate control: guard cell regulation by microbial stress

Abstract

Contents 1049I.1049II.1050III.1055IV.1057V.10581059References1059 Summary Terrestrial plants rely on stomata, small pores in the leaf surface, for photosynthetic gas exchange and transpiration of water. The stomata, formed by a pair of guard cells, dynamically increase and decrease their volume to control the pore size in response to environmental cues. Stresses can trigger similar or opposing movements: for example, drought induces closure of stomata, whereas many pathogens exploit stomata and cause them to open to facilitate entry into plant tissues. The latter is an active process as stomatal closure is part of the plant's immune response. Stomatal research has contributed much to clarify the signalling pathways of abiotic stress, but guard cell signalling in response to microbes is a relatively new area of research. In this article, we discuss present knowledge of stomatal regulation in response to microbes and highlight common points of convergence, and differences, compared to stomatal regulation by abiotic stresses. We also expand on the mechanisms by which pathogens manipulate these processes to promote disease, for example by delivering effectors to inhibit closure or trigger opening of stomata. The study of pathogen effectors in stomatal manipulation will aid our understanding of guard cell signalling.

Direct and Indirect Visualization of Bacterial Effector Delivery into Diverse Plant Cell Types during Infection

“…Stomatal pores on the leaf surface serve as ports of entry into the leaf interior for multiple pathogens, including P. syringae (McLachlan et al, 2014). Several effectors (AvrB, HopX1, HopZ1a, and HopF2) have been shown to interfere with PAMP-induced stomatal closure and promote pathogen entry to the leaf apoplast (Jiang et al, 2013;Gimenez-Ibanez et al, 2014;Hurley et al, 2014; (A) Roots of 4-week-old plants were inoculated with the indicated R. solanacearum genotypes, and disease symptoms were scored 8 d postinoculation.…”

Aquaporins facilitate hydrogen peroxide entry into guard cells to mediate ABA- and pathogen-triggered stomatal closure

“…Signaling pathways inducing stomatal closure in response to ABA and pathogens are increasingly well documented (3,14). We recently proposed that phosphorylation of AtPIP2;1 at Ser121, by OST1 and possibly other protein kinases, is critical for increasing guard cell water transport in response to ABA (11).…”

“…While key proteins such as glutathione peroxidase 3 (AtGPX3) (45) or ABI2 protein phosphatase (46) are known to be regulated through ROS-dependent oxidation, other cellular targets of H 2 O 2 may play an important role during stomatal closure and not restricted to guard cell responses to flg22 and ABA. Ethylene and methyl jasmonate (MeJA) also induce H 2 O 2 production (14,47) to promote stomatal closure, thereby protecting the plant from dehydration and/or pathogen attacks. While AtPIP2;1 is the only detected PIP2 expressed in guard cells (48), several PIP1s are also expressed, which may transport H 2 O 2 (24,30).…”

“…While plants have the capacity to close their stomata after perception of pathogenassociated molecular patterns (PAMPs) or damaged associated molecular patterns (DAMPs) (12), some pathogens can, in turn, thwart the stomatal closure by means of effectors such as coronatine (12) or HoPM1 (13). Signaling pathways involved in guard cell response to pathogens have been the focus of recent studies (14). Notably, flg22 (a PAMP from the bacterium Pseudomonas syringae pv.…”

Fundamental and applied research in ABA signaling: Regulation by ABA of the chromatin remodeling ATPase BRAHMA and biotechnological use of the PP2CA promoter.

“…ABA plays major roles in abiotic and biotic stress responses. It is implicated in guard cell regulation triggering stomatal closure to maintain water balance (Sirichandra et al, 2009, Merilo et al, 2015, Munemasa et al, 2015, antagonizes gibberellins (GAs) effects to fine tune growth in adverse situations (Golldack et al, 2013), controls gene expression to help with plant adaptation to stress (Bechtold et al, 2016) and also has a role in the promotion of plant resistance to pathogens restricting its entrance via stomata (McLachlan et al, 2014). Despite of the well known functions in abiotic and biotic stress, ABA is also important for the regulation of several physiological and developmental events as embryo maturation, promotion of seed desiccation tolerance and dormancy, germination and seedling establishment, primary and lateral root growth and transition from vegetative to reproductive stage (Finkelstein et al, 2002, Cutler et al, 2010, Finkelstein, 2013, Harris, 2015.…”