4.7 Article

Host susceptibility factors render ripe tomato fruit vulnerable to fungal disease despite active immune responses

Journal

JOURNAL OF EXPERIMENTAL BOTANY
Volume 72, Issue 7, Pages 2696-2709

Publisher

OXFORD UNIV PRESS
DOI: 10.1093/jxb/eraa601

Keywords

Botrytis cinerea; fruit-pathogen interactions; fruit ripening; Fusarium acuminatum; immune responses; non-ripening mutants; pectate lyase; preformed defenses; Rhizopus stolonifer; susceptibility factors

Categories

Funding

  1. College of Agricultural and Environmental Sciences
  2. Department of Plant Sciences (UC Davis)
  3. Plant Sciences GSR Award (UC Davis)
  4. BBSRC [BB/J015598/1] Funding Source: UKRI

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This study showed that even susceptible ripe fruit can mount a strong immune response to pathogen infection. Furthermore, gene knockout experiments confirmed that pectate lyase, not polygalacturonase, plays a crucial role in susceptibility of fruit to fungal pathogens.
The increased susceptibility of ripe fruit to fungal pathogens poses a substantial threat to crop production and marketability. Here, we coupled transcriptomic analyses with mutant studies to uncover critical processes associated with defense and susceptibility in tomato (Solanum lycopersicum) fruit. Using unripe and ripe fruit inoculated with three fungal pathogens, we identified common pathogen responses reliant on chitinases, WRKY transcription factors, and reactive oxygen species detoxification. We established that the magnitude and diversity of defense responses do not significantly impact the interaction outcome, as susceptible ripe fruit mounted a strong immune response to pathogen infection. Then, to distinguish features of ripening that may be responsible for susceptibility, we utilized non-ripening tomato mutants that displayed different susceptibility patterns to fungal infection. Based on transcriptional and hormone profiling, susceptible tomato genotypes had losses in the maintenance of cellular redox homeostasis, while jasmonic acid accumulation and signaling coincided with defense activation in resistant fruit. We identified and validated a susceptibility factor, pectate lyase (PL). CRISPR-based knockouts of PL, but not polygalacturonase (PG2a), reduced susceptibility of ripe fruit by >50%. This study suggests that targeting specific genes that promote susceptibility is a viable strategy to improve the resistance of tomato fruit against fungal disease.

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