How do plants defend themselves against bacterial wilt? Understanding tomato responses to the pathogen Ralstonia solanacearum.
Final Report Abstract
Ralstonia solanacearum, the causal agent of bacterial wilt (BW) disease, is a destructive widespread pathogen causing significant global economic and social hardship. Resistance is the only practical way to control bacterial wilt, but the resistance is multigenic and R. solanacearum is representative of a large group of high-impact broad host range plant pathogens that circumvent gene-for-gene recognition. Despite its widespread occurrence and importance in the natural world, little is known about multigenic resistance. Gene expression analysis was used to address this deficiency and elucidate mechanisms that natural hosts like tomato use to defend themselves against R. solanacearum. Tomato plants infected with two ecologically different R. solanacearum strains, temperate race 3 biovar 2 strain UW551 and tropical strain GMI1000, upregulated genes in both the ethylene (ET) and salicylic acid (SA) defense signal transduction pathways. Ethylene-insensitive Never Ripe plants as well as transgenic NahG overexpressing plants depleting endogenous SA were more sensitive to infections than wild-type tomatoes. This confirmed that ET and SA are important for tomato defense responses to R. solanacearum. However, the horizontally wilt-resistant tomato line H7996 activated expression of these defense genes faster and to a greater degree in response to R. solanacearum infection than did susceptible cultivar Bonny Best. Strain UW551 could avoid or calm defense responses in the susceptible tomato cultivar presumably by upregulating genes for Type 3-secreted effectors to a significantly greater degree than GMI1000. Interestingly, temperature significantly affected host defense gene expression. Genes in the ET and SA pathways were more strongly expressed at 20°C than at 28°C in tomato plants with comparable pathogen populations. R. solanacearum produces copious extracellular polysaccharide (EPS), a major virulence factor. The function of EPS in wilt disease is uncertain. Leading hypotheses are that EPS physically obstructs plant water transport, or that EPS cloaks the bacterium from host plant recognition and subsequent defense. Surprisingly, EPS played different roles in resistant and susceptible host responses to R. solanacearum. In susceptible plants the wild-type and eps- mutant strains induced generally similar defense responses. But in resistant H7996 tomato plants, the wild-type pathogens induced significantly greater defense responses than the eps- mutants, suggesting that the resistant host recognizes R. solanacearum EPS. Consistent with this idea, purified EPS elicited significant SA pathway defense gene expression in resistant, but not in susceptible, tomato plants. In addition, the eps- mutant triggered noticeably less production of defense-associated reactive oxygen species in resistant tomato stems and leaves, despite attaining similar cell densities in planta. Collectively, these data suggest that bacterial wilt-resistant plants can specifically recognize EPS from R. solanacearum. Recognition of R. solanacearum EPS, either specifically or as a MAMP, could give BW-resistant H7996 tomato plants a crucial advantage by triggering faster defense responses and thus decrease disease severity. This novel finding represents an important step in understanding the mechanisms of plant disease resistance, leading to better ways to prevent crop losses.
Publications
- 2009. Molecular responses to quantitative bacterial wilt resistance on tomato. Phytopathology 99: S169
Milling, A. and C. Allen
- 2010. Comparative in planta microarray analysis modifies the regulatory model for the type three secretion system in Ralstonia solanacearum. Phytopathology 100: S55
Jacobs, J., L. Babujee, F. Meng, A. Milling and C. Allen
- 2011. Ralstonia solanacearum extracellular polysaccharide is a specific elicitor of defense responses in wilt-resistant tomato plants. PLoS ONE 6: e15853
Milling, A., L. Babujee and C. Allen
