Stomatal immunity against fungal invasion comprises not only chitin-induced stomatal closure but also chitosan-induced guard cell death

Abstract

Many pathogenic fungi exploit stomata as invasion routes, causing destructive diseases of major cereal crops. Intensive interaction is expected to occur between guard cells and fungi. In the present study, we took advantage of well-conserved molecules derived from the fungal cell wall, chitin oligosaccharide (CTOS), and chitosan oligosaccharide (CSOS) to study how guard cells respond to fungal invasion. In Arabidopsis, CTOS induced stomatal closure through a signaling mediated by its receptor CERK1, Ca2+, and a major S-type anion channel, SLAC1. CSOS, which is converted from CTOS by chitin deacetylases from invading fungi, did not induce stomatal closure, suggesting that this conversion is a fungal strategy to evade stomatal closure. At higher concentrations, CSOS but not CTOS induced guard cell death in a manner dependent on Ca2+ but not CERK1. These results suggest that stomatal immunity against fungal invasion comprises not only CTOS-induced stomatal closure but also CSOS-induced guard cell death.

Abscisic Acid-Induced Stomatal Closure: An Important Component of Plant Defense Against Abiotic and Biotic Stress

“…ABA’s ability to induce stomatal closure may not always be due to changes occurring in guard cells’ secondary messengers. For e.g., chitosan, a microbial elicitor, can cause the death of guard cells ( Ye et al, 2020b ), likely to make them non-functional. This aspect is thought-provoking and needs to be examined further using ABA or other hormones, such as SA or MJ.…”

“…However, in presence of flg22 or yeast elicitor, the activity of OST1 did not increase ( Montillet et al, 2013 ; Ye et al, 2015 ). Albeit in a resting stage, OST1 participated in stomatal closure by variety of signals including PAMPs (e.g., flg 22, yeast elicitor, chitosan) or environmental components, such as high CO 2 or high humidity ( Melotto et al, 2006 ; Ye et al, 2015 , 2020b ; Ye and Murata, 2016 ; Pantin and Blatt, 2018 ). Besides its action through ROS/NO/Ca 2+ , OST1 could directly modulate ion channels to cause stomatal closure ( Figure 1 ).…”

“…Also, stomata need to open subsequently to keep up the gas exchange and normal plant function. At the same time, microbial pathogens initiate counteractive measures to reopen stomata, by either effectors, (such as coronatine or fusicoccin, Schulze-Lefert and Robatzek, 2006 ; Gudesblat et al, 2009a ; Melotto et al, 2017 ), locking the open-stomata ( Prats et al, 2006 ) or even killing guard cells to prevent their closure ( Ye et al, 2020b ).…”

Rice Stomatal Mega-Papillae Restrict Water Loss and Pathogen Entry

“…Plant stomata regulate gaseous exchange with the environment, and in some cases prevent pathogens from entering the leaf interior. In the short term, these processes can be regulated via alterations to stomatal pore aperture, and over longer durations, via changes to stomatal size and/or density (Zeiger et al, 1987;Lake and Woodward, 2008;Martin-StPaul et al, 2017;Dutton et al, 2019;Ye et al, 2020). A number of other specialized epidermal adaptions have also evolved that influence airflow and/or pathogen entry in and around stomata, and these include papillae outgrowths (Barthlott et al, 1998;Hückelhoven et al, 1999;Wakte et al, 2007;Mohammadian et al, 2009;Ensikat et al, 2011;Müller et al, 2017).…”

“…This loss of water drives a transpiration stream, permitting evaporative cooling and internal movement of solutes from roots to shoots (Hetherington and Woodward, 2003;Hepworth et al, 2015;Caine et al, 2019). Stomatal closure prevents water loss and mitigates against pathogens which enter through the pore -key traits in conserving water and protecting against disease, but it also prevents CO 2 uptake (Flexas and Medrano, 2002;Martin-StPaul et al, 2017;Ye et al, 2020). Over longer durations, plants can modulate gaseous exchanges and defense against pathogens via changes to stomatal development (Lake et al, 2001;Casson and Gray, 2008;Beerling and Franks, 2009;Dutton et al, 2019).…”