SlWRKY16 and SlWRKY31 of tomato, negative regulators of plant defense, involved in susceptibility activation following root-knot nematode Meloidogyne javanica infection

Abstract

The involvement of WRKY transcription factors in plant-nematode interactions, and in particular, how these WRKYs participate in regulating the complex morphological and physiological changes occurring after nematode infection, are the topic of active research. We characterized the functional role of the unstudied tomato WRKY genes SlWRKY16 and SlWRKY31 in regulating tomato roots’ response to infection by the root-knot nematode Meloidogyne javanica. Using promoter–GUS reporter gene fusions and qRT-PCR, we show that both SlWRKYs are predominantly expressed during the first half of the parasitic life stages, when feeding-site induction and construction occur. Expression of SlWRKY16 increased sharply 15 days after inoculation, whereas SlWRKY31 was already induced earlier, but reached its maximum expression at this time. Both genes were downregulated at the mature female stage. To determine biological function, we produced transgenic lines overexpressing SlWRKY16 and SlWRKY31 in tomato hairy roots. Overexpression of both genes resulted in enhanced M. javanica infection, reflected by increased galling occurrence and reproduction. Expression profiling of marker genes responsive to defense-associated phytohormones indicated reductions in salicylic acid defense-related PR-1 and jasmonic acid defense-related PI in inoculated roots overexpressing SlWRK16 and SlWRKY31, respectively. Our results suggest that SlWRKY16 and SlWRKY31 function as negative regulators of plant immunity induced upon nematode infection.

Network analyses reveal D clade ethylene response factors as major regulators of jasmonic acid-mediated resistance to early blight disease complex in tomato

“…table 4 ). Notable defense related yellow module GRN hub genes are SlWRKY28 [91], SlWRKY31 [92], and SlWRKY53 [93].…”

“…The yellow module yielded one TF as a hub gene in its co-expression network, SlWRKY16 . It has been shown be a susceptibility factor to nematode parasitism [92], but also to increase lignification and successfully induce resistance to field dodder [97], and is upregulated during ETI of Pst DC3000 [80]. It is expressed in all 3 treatments however, and therefore represents either an insufficient defense mechanism, or its expression is abolished after 3 hpi by virulent EBDC so that it can no longer contribute to the defense response.…”

“…table 5 ). SlWRKY31 is also a yellow module GRN hub gene, and it was also found to suppress nematode defenses by Kumar et al [92] . In our dataset SlWRKY16 is expressed in all treatments and SlWRKY31 has very low expression in general, giving neither of them explanatory power to produce susceptibility to 1117-1 and defense to CS046.…”

Functional studies of plant transcription factors and their relevance in the plant root-knot nematode interaction

“…Both genes were induced during nematode infection until late infection stages (28 dpi). Overexpression of these genes in tomato lines using R. rhizogenes -mediated transformation under the control of the CaMV35S promoter resulted in increased susceptibility to M. javanica , as evidenced by enhanced galling and reproduction parameters ( Kumar et al., 2023 ; Table 1 ).…”

SlWRKY81 regulates Spd synthesis and Na+/K+ homeostasis through interaction with SlJAZ1 mediated JA pathway to improve tomato saline‐alkali resistance

“…The ability of WRKY genes to enhance resistance to saline‐alkali stress has also been documented by investigations on crops, such as Populus trichocarpa (Niu et al., 2021) and Trollius chinensis (Hou et al., 2023). A total of 83 SlWRKY genes exist in tomato, many of which are induced by various abiotic stresses (Kumar et al., 2023). SlWRKY3 enhances the salt stress resistance of tomato seedlings (Hichri et al., 2017), whereas SlWRKY42 enhances the aluminum toxicity tolerance of tomato by positively regulating the malate transporter SlALMT9 (Ye et al., 2017).…”