Drought Stress Interacts With Powdery Mildew Infection in Tomato

Abstract

Under field conditions, plants are often exposed to more than one stress factor at the same time, and therefore need to adapt to different combinations of stresses. Crosstalk between responses to abiotic and biotic stresses is known to occur, and the interaction between stress responses can be positive or negative. We studied the interaction of drought stress and powdery mildew (PM) infection in tomatoes using near-isogenic tomato lines (NILs) carrying the Ol-1, ol-2, or Ol-4 gene that confers resistance to tomato PM caused by Oidium neolycopersici. Our study demonstrated that drought-induced growth reduction was not further reduced by powdery mildew infection. Drought stress, however, decreased fungal infection in the susceptible genotype Moneymaker (MM) with fungal biomass tending to decrease further as the drought severity increased. Drought stress did not affect PM resistance levels of resistant NIL carrying ol-2 (a mutant of the tomato susceptibility Mlo gene) and Ol-4 an NLR (nucleotide-binding site-LRR) R gene associated with a fast hypersensitivity response (HR) but tended to slightly decrease disease levels of NIL-Ol-1 (no gene characterized yet, associated with a slow HR following PM infection). At the molecular level, genes involved in abscisic acid (ABA), salicylic acid (SA), and ethylene pathways were highly induced under combined stress indicating the involvement of ABA, SA, and ethylene in the crosstalk between abiotic and biotic stress. Messenger RNA expression of the ABA-responsive dehydrin SlTAS14 was induced under drought and combined stress with the highest induction under combined stress, and resistant NIL lines showed higher expression levels than MM. The expression of SlNCED (involved in ABA synthesis) was also upregulated under drought and highly induced under combined stress. Expression levels of pathogen responsive gene SlPR1 (an indicator of the SA pathway) and SlACS (involved in ethylene synthesis) were highly induced under powdery mildew infection in MM and the Ol-1 and were induced the most under combined stress in these lines. Taken together, these findings indicate that drought stress can interact with and influence PM infection in tomatoes in a resistance type-dependent manner. The role of hormonal signaling pathways in the crosstalk between drought stress and PM infection is further discussed.

Overexpression of the C4 protein of tomato yellow leaf curl Sardinia virus increases tomato resistance to powdery mildew

“…at early stages of infection and fits also with the behavior of plants at late infection stages, as previously predicted (Prokopováet al, 2010). Interestingly, the attenuated CCI decrease here observed for TYLCSV C4 plants challenged by On is in line with the results reported for tomato lines resistant to PM, which were obtained following partial introgression of the PM resistance genes Ol, such as the Ol-1 and Ol-4 (Bai et al, 2005); these plants were partially resistant to On when subjected to mild or severe drought stress (Sunarti et al, 2022), suggesting the hypothesis that C4 mimics the priming of drought stress imposition on fungal infection. Moreover, the lower impact of On infection on plant height observed for C4 plants compared to WT individuals is in line with the results of the Arabidopsis line pmr4-1 and the tomato line Ol-1, displaying partial PM resistance upon fungal inoculation (Nishimura et al, 2003;Sunarti et al, 2022).…”

“…Altogether, the level of On symptom reduction here described for TYLCSV C4-expressing tomato plants is similar to that reported for the Arabidopsis line pmr4-1 (Nishimura et al, 2003) and the tomato Ol-1 line (Sunarti et al, 2022).…”

“…Specifically, SA is considered the primary phytohormone that mediates resistance against biotrophic pathogens (An and Mou, 2011), while JA is primarily responsible for regulating defense responses against necrotrophic pathogens and herbivores (Wasternack, 2007). SA-dependent disease resistance was reported in the case of the PM-resistant 4 (pmr4) Arabidopsis mutant line (Nishimura et al, 2003) and in the PM partially resistant tomato line carrying the Ol-1 resistance gene when subjected to single (PM) or combined (PM and drought) stress (Sunarti et al, 2022). In the last decade, the biochemical processes underlying the infection and the resistance responses of tomato plants to On are being investigated, including the role not only of hormones (Achuo et al, 2004;Li et al, 2012), reactive oxygen species (ROS) (Mlıćkováet al, 2004;Tomańkovaé t al., 2006), and reactive nitrogen species (Piterkováet al, 2009;, but also of elicitors (oligandrin, BABA) (Satkováet al, 2017), whose effect can be related either to effectortriggered immunity (ETI) or to pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI).…”

Overview of Repressive miRNA Regulation by Short Tandem Target Mimic (STTM): Applications and Impact on Plant Biology

“…The tomato is a self-pollinated crop in the Solanaceae family with around 3000 species, and is the second highest in global vegetable production, after the potato [ 83 ]. Tomato plants become more resistant to powdery mildew if treated with drought, indicating plant resistance crosstalk to be more resistant toward other stresses [ 84 ]. In addition, STTM1916-transformed tomato plants are made more resistant to two bacterial infections, Phytophthora infestans and Botrytis cinerea , by upregulating strictosidine synthase ( STR-2 ), UDP-glycosyltransferase ( UGT ), and MYB transcription factor MYB12 [ 85 ].…”

Solanum lycopersicum, a Model Plant for the Studies in Developmental Biology, Stress Biology and Food Science

“…Using the near-isogenic lines (NILs) carrying the resistance genes Ol-1 , Ol-2 and Ol-4 to Oidium neolycopersici , Sunarti et al revealed that the growth reduction caused by drought stress was not further aggravated upon powdery mildew (PM) infection, while more severe drought stress resulted in less biomass of PM. Upon drought stress, the NILs harboring Ol-2 , and Ol-4 displayed normal resistance and cell death phenotype, while the NIL carrying Ol-1 showed mildly attenuated resistance [ 60 ]. Interestingly, many genes related to hormonal signaling and wound responses, such as SlNCED , SlPR1 , SlACS2 and SlLIN6 , were significantly induced, further implying a complex cross-talk of abscisic acid (ABA), salicylic acid (SA), jasmonic acid (JA), ethylene (ET) and wound signaling during combined stress conditions.…”