Solanaceous plants switch to cytokinin‐mediated immunity against Ralstonia solanacearum under high temperature and high humidity

Abstract

Plant diseases generally tend to be more serious under conditions of high temperature and high humidity (HTHH) than under ambient temperature, but plant immunity against pathogen attacks under HTHH remains elusive. Herein, we used pepper as an example to study how Solanaceae cope with Ralstonia solanacearum infection (RSI) under HTHH by performing RNA‐seq combined with the reverse genetic method. The result showed that immunities mediated by salicylic acid (SA) and jasmonic acid (JA) in pepper roots were activated by RSI under ambient temperature. However, upon RSI under HTHH, JA signalling was blocked and SA signalling was activated early but its duration was greatly shortened in pepper roots, instead, expression of CaIPT5 and Glutathione S‐transferase encoding genes, as well as endogenous content of trans‐Zeatin, were enhanced. In addition, by silencing in pepper plants and overexpression in Nicotiana benthamiana, CaIPT5 was found to act positively in the immune response to RSI under HTHH in a way related to CaPRP1 and CaMgst3. Furthermore, the susceptibility of pepper, tomato and tobacco to RSI under HTHH was significantly reduced by exogenously applied tZ, but not by either SA or MeJA. All these data collectively suggest that pepper employs cytokinin‐mediated immunity to cope with RSI under HTHH.

Climate change impedes plant immunity mechanisms

“…CK can also increase susceptibility to pathogens not only by inhibiting the plant immune system (i.e., PTI and ROS) but also by establishing source-sink relationships (Albrecht and Argueso, 2017;McIntyre et al, 2021). In pepper (Capsicum annuum), Yang et al showed that infection with Ralstonia solanacearum, a hemibiotrophic pathogen causing bacterial wilt, activates SA signaling at an early stage and JA signaling at a later stage in roots at ambient temperature, but these responses are both impaired at high temperature (Yang et al, 2022). Instead, isopentenyltransferase (IPT) genes, including CaIPT5, encoding a critical enzyme in cytokinin biosynthesis, were upregulated by R. solanacearum infection under high temperature.…”

“…Instead, isopentenyltransferase (IPT) genes, including CaIPT5, encoding a critical enzyme in cytokinin biosynthesis, were upregulated by R. solanacearum infection under high temperature. Surprisingly, exogenous treatment with transzeatin (tZ), the bioactive CK, significantly enhanced disease resistance to R. solanacearum in pepper, tomato, and tobacco (Nicotiana benthamiana) under high temperature, while SA and JA did not (Yang et al, 2022). Moreover, the authors suggested that CK triggers chromatin remodeling, resulting in the upregulation of genes encoding glutathione S-transferase (e.g., CaPRP1 and CaMgst3) and downregulation of genes involved in SA and JA signaling (e.g., CaSTH2 and CaDEF1 (Yang et al, 2022).…”

“…A recent study revealed that the phytohormone cytokinin (CK) also plays an important role in plant immunity at high temperatures ( Yang et al., 2022 ). The trade-off between growth and defense modulated by CK can result in opposite effects on plant–pathogen interactions ( Choi et al., 2011 ).…”

“…In pepper ( Capsicum annuum ), Yang et al. showed that infection with Ralstonia solanacearum , a hemibiotrophic pathogen causing bacterial wilt, activates SA signaling at an early stage and JA signaling at a later stage in roots at ambient temperature, but these responses are both impaired at high temperature ( Yang et al., 2022 ). Instead, isopentenyltransferase ( IPT ) genes, including CaIPT5 , encoding a critical enzyme in cytokinin biosynthesis, were upregulated by R .…”

The CaPti1–CaERF3 module positively regulates resistance of Capsicum annuum to bacterial wilt disease by coupling enhanced immunity and dehydration tolerance

“…Previous studies have shown that serine/threonine protein kinases (S_TKc) play vital roles during plant responses to pathogen attack. To identify candidate pepper genes encoding the S_TKc kinase involved in the response to R. solanacearum and ABA treatment, we analyzed the expression profiles of S_TKc genes in pepper plants exposed to R. solanacearum and ABA treatment based on publicly available data from the Pepper Hub (http:/http://www.hnivr.org/) (Liu et al., 2017) and our published transcriptome deep‐sequencing (RNA‐seq) data in pepper plants challenged with R. solanacearum inoculation via root irrigation (Yang et al., 2021). One S_TKc gene was significantly upregulated by both R. solanacearum and ABA exposure.…”