Tomato yellow leaf curl virus infection mitigates the heat stress response of plants grown at high temperatures

Abstract

Cultured tomatoes are often exposed to a combination of extreme heat and infection with Tomato yellow leaf curl virus (TYLCV). This stress combination leads to intense disease symptoms and yield losses. The response of TYLCV-susceptible and resistant tomatoes to heat stress together with viral infection was compared. The plant heat-stress response was undermined in TYLCV infected plants. The decline correlated with the down-regulation of heat shock transcription factors (HSFs) HSFA2 and HSFB1, and consequently, of HSF-regulated genes Hsp17, Apx1, Apx2 and Hsp90. We proposed that the weakened heat stress response was due to the decreased capacity of HSFA2 to translocate into the nuclei of infected cells. All the six TYLCV proteins were able to interact with tomato HSFA2 in vitro, moreover, coat protein developed complexes with HSFA2 in nuclei. Capturing of HSFA2 by viral proteins could suppress the transcriptional activation of heat stress response genes. Application of both heat and TYLCV stresses was accompanied by the development of intracellular large protein aggregates containing TYLCV proteins and DNA. The maintenance of cellular chaperones in the aggregated state, even after recovery from heat stress, prevents the circulation of free soluble chaperones, causing an additional decrease in stress response efficiency.

Differences and commonalities of plant responses to single and combined stresses

“…Generally, pathogenic infections have been found to weaken plant tolerance to abiotic stress. For instance, tomato plants infected with Tomato Yellow Leaf Curl Virus are more susceptible to heat (Anfoka et al ., ). This increased heat susceptibility has been associated with a downregulation of heat‐shock factors and proteins.…”

The six Tomato yellow leaf curl virus genes expressed individually in tomato induce different levels of plant stress response attenuation

“…Furthermore, TYLCV is able to mitigate CD caused by other factors such as the inactivation of the HSP90 machinery . TYLCV-dependent suppression of the plant heat stress response was demonstrated to occur through the downregulation of HSFA2 expression (Anfoka et al 2016), which controls key aspects of the stress response (especially heat stress) by regulating the transcription activity of a wide range of genes involved in numerous signaling and metabolic pathways (von Koskull-Döring et al 2007). …”

“…Similar changes of protein and RNA patterns were detected not only for HSFA2, but also for HSFA2-regulated HSP17. An in vitro protein-protein complex between tomato HSFA2 and viral proteins has been already described (Anfoka et al 2016). All the six TYLCV proteins were able to capture one of the main cellular regulators of the stress response.…”

“…4b). In TYLCV susceptible tomatoes, the virus amount constantly increased until it reached a plateau maintained for up to 60 dpi (Gorovits et al 2013a;Anfoka et al 2016). In infected Hsp90-silenced tomatoes, despite the plant decline being partially suppressed by TYLCV infection, virus CP and DNA accumulated at least until 35 dpi ; Fig.…”

The C4 protein from the geminivirus Tomato yellow leaf curl virus confers drought tolerance in Arabidopsis through an ABA‐independent mechanism

“…Plants have adopted a wide range of strategies to confront the negative effects of drought, including increasing water uptake by optimizing the root system, closing stomata to limit the water loss caused by transpiration, accumulating osmoprotectants, or producing the hormone abscisic acid (ABA). This intricate scenario makes drought resistance a highly complex trait, with polygenic nature, low heritability, and vastly influenced by genotypeenvironment interactions (Fang and Xiong, 2014).A growing body of evidence indicates that viral infections can result in improved plant tolerance to abiotic stresses (see, among others: Aguilar et al, 2017;Anfoka et al, 2016;Westwood et al, 2012;Xu et al, 2008), raising the tantalizing idea that the identification of the molecular mechanisms underlying these viral effects could unlock yet-unknown stress tolerance strategies and pave the way for the generation of stress-resilient plants. Geminiviruses are viruses with small circular, single-stranded DNA genomes that infect a broad range of plants.…”