Opposing effects on two phases of defense responses from concerted actions of HSC70 and BON1 in Arabidopsis

Abstract

The plant immune system consists of multiple layers of responses targeting various phases of pathogen infection. Here, we provide evidence showing that two responses, one controlling stomatal closure and the other mediated by intracellular receptor proteins, can be regulated by the same proteins but in an antagonistic manner. The HEAT SHOCK COGNATE70 (HSC70), while previously known as a negative regulator of stomatal closure, is a positive regulator of immune responses mediated by the immune receptor protein SUPPRESSOR OF NPR1-1, CONSTITUTIVE1 (SNC1) as well as basal defense responses. In contrast to HSC70, a calcium-binding protein, BONZAI1 (BON1), promotes abscisic acid-and pathogen-triggered stomatal closure in addition to and independent of its previously known negative role in SNC1 regulation. BON1 likely regulates stomatal closure through activating SUPPESSOR OF THE G2 ALLELE OF SKP1 VARIANT B and inhibiting HSC70. New functions of BON1 and HSC70 identified in this study thus reveal opposite effects of each of them on immunity. The opposing roles of these regulators at different phases of plant immune responses exemplify the complexity in immunity regulation and suggest that immune receptors may guard positive regulators functioning at stomatal closure control.

Albino Leaf 1 that Encodes the Sole Octotricopeptide Repeat Protein Is Responsible for Chloroplast Development in Rice

“…Arabidopsis (Arabidopsis thaliana) rap mutants (SAIL_1223_C10) were obtained from the Nottingham Arabidopsis Stock Centre. Arabidopsis seeds were grown as described previously (Gou et al, 2015).…”

Calcium Pumps and Interacting BON1 Protein Modulate Calcium Signature, Stomatal Closure, and Plant Immunity

“…In addition to the function in negatively regulating SNC1, BON1 has been recently shown to promote stomatal closure in response to stimuli, including abscisic acid and bacterial pathogen (Gou et al, 2015). This function is independent of SNC1 or NB-LRR signaling, and the bon1 mutant is defective in stomatal closure when autoimmunity is suppressed by the SNC1 LOF mutation snc1-11 (Gou et al, 2015). Therefore, BON1 has a more general role in regulating signaling events in addition to NLR gene expression.…”

“…However, these observed defects are dependent on a Col-0 specific NB-LRR (Nucleotide Binding-Leucine Rich Repeat) gene, SNC1, and the LOF bon1-2 allele in the Wassilewakija (Ws) accession does not exhibit constitutive defense activation because there is no functional SNC1 in Ws (Yang and Hua, 2004). In addition to the function in negatively regulating SNC1, BON1 has been recently shown to promote stomatal closure in response to stimuli, including abscisic acid and bacterial pathogen (Gou et al, 2015). This function is independent of SNC1 or NB-LRR signaling, and the bon1 mutant is defective in stomatal closure when autoimmunity is suppressed by the SNC1 LOF mutation snc1-11 (Gou et al, 2015).…”

“…The altered calcium signature in bon1, aca10, and aca8 guard cells suggests that these mutants might have defects in stomata closure in response to environmental stimuli. Indeed, the bon1 mutant does not close stomata in response to calcium, abscisic acid, or pathogen, and this defect is not a consequence of autoimmunity as it is independent of SNC1 or PAD4 (Gou et al, 2015;Fig. 8A).…”

“…Five of them encode calcium efflux pumps, including ACA1, ACA2, ACA10, ACA11, and ACA.1. Previously, ACA.1 was identified as a putative BON1-interacting protein by BON1 immunoprecipitation followed by mass spectrometry (Gou et al, 2015), suggesting that BON1 could physically interact with ACA proteins. Because ACA1, 2, and 11 are localized to the plastid envelope, ER, and vacuole, respectively (Huang et al, 1993;Harper et al, 1998;Lee et al, 2007), we chose the PM-localized ACA10 for further analysis because BON1 is PM localized.…”