YODA Kinase Controls a Novel Immune Pathway of Tomato Conferring Enhanced Disease Resistance to the Bacterium Pseudomonas syringae

Abstract

Mitogen-activated protein kinases (MAPK) play pivotal roles in transducing developmental cues and environmental signals into cellular responses through pathways initiated by MAPK kinase kinases (MAP3K). AtYODA is a MAP3K of Arabidopsis thaliana that controls stomatal development and non-canonical immune responses. Arabidopsis plants overexpressing a constitutively active YODA protein ( AtCA-YDA ) show broad-spectrum disease resistance and constitutive expression of defensive genes. We tested YDA function in crops immunity by heterologously overexpressing AtCA-YDA in Solanum lycopersicum . We found that these tomato AtCA-YDA plants do not show developmental phenotypes and fitness alterations, except a reduction in stomatal index, as reported in Arabidopsis AtCA-YDA plants. Notably, AtCA-YDA tomato plants show enhanced resistance to the bacterial pathogen Pseudomonas syringae pv. tomato DC3000 and constitutive upregulation of defense-associated genes, corroborating the functionality of YDA in tomato immunity. This function was further supported by generating CRISPR/Cas9-edited tomato mutants impaired in the closest orthologs of AtYDA [ Solyc08g081210 ( SlYDA1 ) and Solyc03g025360 ( SlYDA2 )]. Slyda1 and Slyda2 mutants are highly susceptible to P. syringae pv. tomato DC3000 in comparison to wild-type plants but only Slyda2 shows altered stomatal index. These results indicate that tomato orthologs have specialized functions and support that YDA also regulates immune responses in tomato and may be a trait for breeding disease resistance.

MAP kinase cascades in plant development and immune signaling

“…YDA is closely related to MAPKKK3/5 and regulates MPK3/6 activation in plant development. It was recently reported to regulate defense response as well (Sopeña‐Torres et al , 2018; Téllez et al , 2020). However, flg22‐induced MAPK activation is enhanced in a partial loss‐of‐function mutant of YDA and YDA silencing lines (Sopeña‐Torres et al , 2018; Sun et al , 2018).…”

Green leaf volatiles co‐opt proteins involved in molecular pattern signalling in plant cells

“…Tomato Sl YODAs also function in immunity. The tomato yda1 and yda2 mutants exhibited a compromised immune response to bacterial pathogens (Téllez et al, 2020), and all three Sl YDA genes are upregulated in response to P. syringae infection (Wu, Wang, et al, 2014). In Arabidopsis, a target of both the YDA and MAPKKK3/5 cascades is MPK6, the ortholog of tomato MPK1 and MPK2 (Zhang & Zhang, 2022).…”

Green leaf volatiles co-opt proteins involved in molecular pattern signaling in plant cells

“…Tomato Sl YODAs also function in immunity. The tomato yda1 and yda2 mutants exhibited a compromised immune response to bacterial pathogens 57 , and all three Sl YDA genes are upregulated in response to P. syringae infection 58 . In Arabidopsis, a target of both the YDA and MAPKKK3/5 cascades is MPK6, the ortholog of tomato MPK1 and MPK2 59 .…”

“…Tomato SlYODAs also function in immunity. The tomato yda1 and yda2 mutants exhibited a compromised immune response to bacterial pathogens 57 , and all three SlYDA genes are upregulated in response to P. syringae infection 58 .…”