Key Laboratory for Bio-resource and Eco-environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, 610065, China.
Plant J. 2024 Aug;119(4):1967-1985. doi: 10.1111/tpj.16901. Epub 2024 Jun 30.
Female willows exhibit greater drought tolerance and benefit more from exogenous acetic acid (AA)-improved drought tolerance than males. However, the potential mechanisms driving these sex-specific responses remain unclear. To comprehensively investigate the sexually dimorphic responsive mechanisms of willows to drought and exogenous AA, here, we performed physiological, proteomic, Lys-acetylproteomic, and transgenic analyses in female and male Salix myrtillacea exposed to drought and AA-applicated drought treatments, focusing on protein abundance and lysine acetylation (LysAc) changes. Drought-tolerant females suffered less drought-induced photosynthetic and oxidative damage, did not activate AA and acetyl-CoA biosynthesis, TCA cycle, fatty acid metabolism, and jasmonic acid signaling as strongly as drought-sensitive males. Exogenous AA caused overaccumulation of endogenous AA and inhibition of acetyl-CoA biosynthesis and utilization in males. However, exogenous AA greatly enhanced acetyl-CoA biosynthesis and utilization and further enhanced drought performance of females, possibly determining that AA improved drought tolerance more in females than in males. Interestingly, overexpression of acetyl-CoA synthetase (ACS) could reprogram fatty acids, increase LysAc levels, and improve drought tolerance, highlighting the involvement of ACS-derived acetyl-CoA in drought responses. In addition, drought and exogenous AA induced sexually dimorphic LysAc associated with histones, transcription factors, and metabolic enzymes in willows. Especially, exogenous AA may greatly improve the photosynthetic capacity of S. myrtillacea males by decreasing LysAc levels and increasing the abundances of photosynthetic proteins. While hyperacetylation in glycolysis, TCA cycle, and fatty acid biosynthesis potentially possibly serve as negative feedback to acclimate acetyl-CoA biosynthesis and utilization in drought-stressed males and AA-applicated females. Thus, acetyl-CoA biosynthesis and utilization determine the sexually dimorphic responses of S. myrtillacea to drought and exogenous AA.
柳树雌株比雄株具有更强的耐旱性,并能从外源乙酸(AA)提高耐旱性中获益更多。然而,驱动这些性别特异性响应的潜在机制尚不清楚。为了全面研究柳树对干旱和外源 AA 的性别二态响应机制,我们对暴露于干旱和 AA 处理的雌雄山杨进行了生理、蛋白质组学、Lys-乙酰化蛋白质组学和转基因分析,重点研究了蛋白质丰度和赖氨酸乙酰化(LysAc)的变化。耐旱性雌株受干旱诱导的光合作用和氧化损伤较小,不像敏感的雄株那样强烈激活 AA 和乙酰辅酶 A 生物合成、三羧酸循环、脂肪酸代谢和茉莉酸信号。外源 AA 导致内源性 AA 过度积累,并抑制雄性乙酰辅酶 A 的生物合成和利用。然而,外源 AA 极大地增强了乙酰辅酶 A 的生物合成和利用,进一步提高了雌性的耐旱性,这可能决定了 AA 对雌性的耐旱性改善比对雄性的更大。有趣的是,乙酰辅酶 A 合成酶(ACS)的过表达可以重编程脂肪酸,增加 LysAc 水平,并提高耐旱性,突出了 ACS 衍生的乙酰辅酶 A 在耐旱响应中的作用。此外,干旱和外源 AA 诱导了柳树中性别二态性的 LysAc 与组蛋白、转录因子和代谢酶相关。特别是,外源 AA 可能通过降低 LysAc 水平和增加光合蛋白的丰度来极大地提高山杨雄性的光合作用能力。而糖酵解、三羧酸循环和脂肪酸生物合成中的过度乙酰化可能作为负反馈,适应干旱胁迫下雄性和外源 AA 处理下雌性的乙酰辅酶 A 生物合成和利用。因此,乙酰辅酶 A 的生物合成和利用决定了山杨对干旱和外源 AA 的性别二态响应。