Whirly1 enhances tolerance to chilling stress in tomato via protection of photosystem II and regulation of starch degradation

Abstract

Summary In plants, the chilling response involves decreased photosynthetic capacity and increased starch accumulation in chloroplasts. However, the mechanisms that modulate these processes remain unclear. We found that the SlWHY1 gene is significantly induced by chilling stress (4°C) in tomato. Three SlWHY1 overexpression (OE) lines grew better than the wild type (WT) under chilling stress; the OE plants retained intact photosynthetic grana lamellae and showed enhanced hydrolysis of starch. By contrast, RNAi lines that inhibited SlWHY1 were more affected than the corresponding WT cultivar. Their grana lamellae were damaged and starch content increased. The psbA gene encodes the key photosystem II (PSII) protein D1. We show that SlWHY1 binds to the upstream region (A/GTTACCCT/A) of SlpsbA and enhances the de novo synthesis of D1 in chloroplasts. Additionally, SlWHY1 regulates the expression of the starch‐degrading enzyme α‐amylase (SlAMY3‐L) and the starch synthesis‐related enzyme isoamylase gene (SlISA2) in the nucleus, thus modulating the starch content in chloroplasts. We demonstrate that SlWHY1 enhances the resistance of tomato to chilling stress by maintaining the function of PSII and degrading starch. Thus, overexpression of WHY1 may be an effective strategy for enhancing resistance to chilling stress of chilling‐sensitive crops in agricultural production.

Effects of Chilling on the Structure, Function and Development of Chloroplasts

“…Chilling interferes with the normal replacement rate of D1 in the turnover-repair cycle, which results in more serious photodamage ( Allen and Ort, 2001 ). In tomato, the expression of the coding gene of D1 is regulated by SlWHY1 , which is significantly induced by chilling ( Zhuang et al, 2018 ). For a long time, scientists believed that PSII was the main component of photoinhibition.…”

“…Over time, a series of symptoms emerge, including darkening of the stroma, unstacking of the grana, disintegration of the thylakoid membranes and the chloroplast envelope, vesicle accumulation, and chloroplast disintegration ( Musser et al, 1984 ; Kratsch and Wise, 2000 ; Zbierzak et al, 2013 ; Karim et al, 2014 ). In chilling-resistant plants, starch granules continue to decrease over time and finally disappear ( Kratsch and Wise, 2000 ; Zhuang et al, 2018 ), and more condensed grana disks are present ( Garstka et al, 2007 ). As time increases, a cold acclimation process is initiated, and a broad range of responses contribute to the adaptation of plants to chilling stress.…”

H2O2 as a Feedback Signal on Dual-Located WHIRLY1 Associates with Leaf Senescence in Arabidopsis

“…The WHY1 protein bound to the promoter of WRKY53 in a development-dependent manner during early senescence in Arabidopsis [23], while in barley the ortholog could activate the HvS40 gene during natural and stress-related senescence [24]. In tomato, ortholog WHY1 regulated the SlPsbA gene in response to chilling treatment [25]. The involvement of WHY1 protein in modulating telomere length by binding to the AT-rich region of telomeres has also been suggested [26].…”

The Role of Chloroplast Gene Expression in Plant Responses to Environmental Stress

“…Tomato ( Solanum lycopersicum ) WHIRLY1 (SlWHY1) was recently found to upregulate psbA transcription under chilling conditions. Under these conditions, the chloroplast-localized SlWHY1 promotes the transcription of psbA by directly binding to the upstream region of its promoter (the sequence “GTTACCCT”), resulting in increased D1 abundance to relieve photoinhibition [ 69 , 70 ]. Overexpression of SlWHY1 leads to increased de novo synthesis of D1 protein and increased resistance to photoinhibition under chilling conditions [ 69 ].…”

“…Under these conditions, the chloroplast-localized SlWHY1 promotes the transcription of psbA by directly binding to the upstream region of its promoter (the sequence “GTTACCCT”), resulting in increased D1 abundance to relieve photoinhibition [ 69 , 70 ]. Overexpression of SlWHY1 leads to increased de novo synthesis of D1 protein and increased resistance to photoinhibition under chilling conditions [ 69 ]. These findings suggest that psbA transcription is an important target for regulating PSII activity to adjust plant resistance to environmental stresses.…”