Defense responses regulated by jasmonate and delayed senescence caused by ethylene receptor mutation contribute to tolerance of petunia to Botrytis cinerea

Authors: WANG, HONG - University Of California; LIU, GANG - Nanjing Agricultural University; LI, CHUNXIA - Nanjing Agricultural University; Jiang, Cai-Zhong; REID, MICHAEL - University Of California; ZHANG, ZHEN - Nanjing Agricultural University; POWELL, ANN - University Of California

Submitted to: Molecular Plant Pathology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/26/2013
Publication Date: 5/15/2013
Publication URL: http://onlinelibrary.wiley.com/doi/10.1111/mpp.12017/full
Citation: Wang, H., Liu, G., Li, C., Jiang, C., Reid, M.S., Zhang, Z., Powell, A.L. 2013. Defense responses regulated by jasmonate and delayed senescence caused by ethylene receptor mutation contribute to tolerance of petunia to Botrytis cinerea. Molecular Plant Pathology. 14(5):453-469.

Interpretive Summary: Ethylene and jasmonate (JA) have powerful effects on plant disease tolerance pathways through the activation of ethylene or JA responses when plants are challenged by pathogens. The inducible promoter-regulated expression of the Arabidopsis ethylene receptor mutation ethylene-insensitive1-1 (etr1-1) causes ethylene insensitivity in the petunia. To investigate the molecular mechanisms involved in transgenic petunia responses to Botrytis cinerea related to the ethylene and JA pathways, etr1-1 expressing petunias were inoculated with Botrytis cinerea. Induced expression of etr1-1 by a chemical inducer dexamethasone resulted in retarded senescence and reduced disease symptoms on detached leaves and flowers or intact plants. The extent of decreased disease symptoms correlated positively with etr1-1 expression. The JA pathway, independently of the ethylene pathway, activated PhERF expression and consequent defense-related gene expression. These results demonstrate that ethylene induced by biotic stress influences senescence, and that jasmonate in combination with delayed senescence by etr1-1 expression alters tolerance to pathogens.

Technical Abstract: The death of cells can be a programmed event that occurs when plants are attacked by pathogens. Botrytis cinerea (B. cinerea), a model necrotrophic pathogen, triggers the host cell death response because it produces toxins. A hypersensitive reaction (HR) occurs at the site of contact. In Arabidopsis, the HR facilitates further infection with B. cinerea. For the full pathogenicity of B. cinerea in tobacco, an HR is required. Furthermore, delayed or reduced cell death Arabidopsis mutants are more resistant to B. cinerea than wild type plants. Ethylene, a gaseous hormone, regulates different processes during the lifetime of the plant. Ethylene is involved in regulating programmed cell death (PCD) during plant-pathogen interactions. Ethylene participates in cell death processes, as shown in the Arabidopsis lesion mimic mutant vad1-1 affecting ethylene-insensitive4 (EIN4). Ethylene perception and signaling transduction have significant roles in mediating the effects of ethylene during senescence. Ethylene also participates in plant defense responses to pathogens. Ethylene perception and signaling mutants have different disease symptoms when challenged by pathogens; some responses lead to resistance or susceptibility, but the response can also be the same as in wild type plants. For example, the ethylene-insensitive tomato mutant Never ripe (Nr) has the same visible symptoms as wild type plants infected by B. cinerea, but is more resistant to Fusarium oxysporum. Regardless of the differences in plant responses to a pathogen, exposure to and perception of ethylene is known to activate plant defense-related proteins such as the pathogenesis-related proteins (PRs). These proteins are also known to be activated by the jasmonate (JA) pathway of plant responses. Jasmonates are involved in mediating plant responses to pathogens, and can act synergistically with or independently of ethylene in different plants, especially when attacked by necrotrophic pathogens. Ethylene-insensitive1-1 (etr1-1) expressing plants are insensitive to ethylene. Here, we used a reproducible and comprehensive B. cinerea infection system on petunia plants in which etr1-1 was inducibly expressed. We investigated the disease symptoms of intact plants, detached flowers and leaves from two transgenic lines with different levels of etr1-1 expression. The analysis measured the proportion of expanding lesions, the lesion growth rate, disease severity and disease incidence. We also compared the effects of B. cinerea infection on the PCD response in these lines. Our objective was to determine (1) the role of induced etr1-1 expression on senescence induced by biotic stress, i.e. B. cinerea infection, and (2) the roles of ethylene and JA during petunia responses to B. cinerea. Induced expression of etr1-1 by a chemical inducer dexamethasone resulted in retarded senescence and reduced disease symptoms on detached leaves and flowers or intact plants. The extent of decreased disease symptoms correlated positively with etr1-1 expression. The JA pathway, independently of the ethylene pathway, activated PhERF expression and consequent defense-related gene expression. These results demonstrate that ethylene induced by biotic stress influences senescence, and that jasmonate in combination with delayed senescence by etr1-1 expression alters tolerance to pathogens.