Genetic Improvement for Fruits and Vegetables Laboratory, Beltsville Agricultural Research Center, U.S. Department of Agriculture-Agricultural Research Service, Beltsville, MD 20705, USA.
Methods and Application of Food Composition Laboratory, Beltsville Agricultural Research Center, U.S. Department of Agriculture-Agricultural Research Service, Beltsville, MD 20705, USA.
J Exp Bot. 2023 Jun 27;74(12):3700-3713. doi: 10.1093/jxb/erad108.
Anthracnose is a widespread plant disease caused by various species of the fungal pathogen Colletotrichum. In solanaceous plants such as tomato (Solanum lycopersicum), Colletotrichum infections exhibit a quiescent, asymptomatic state in developing fruit, followed by a transition to necrotrophic infections in ripe fruit. Through analysis of fruit tissue extracts of 95L368, a tomato breeding line that yields fruit with enhanced anthracnose resistance, we identified a role for steroidal glycoalkaloids (SGAs) in anthracnose resistance. The SGA α-tomatine and several of its derivatives accumulated at higher levels, in comparison with fruit of the susceptible tomato cultivar US28, and 95L368 fruit extracts displayed fungistatic activity against Colletotrichum. Correspondingly, ripe and unripe 95L368 fruit displayed enhanced expression of glycoalkaloid metabolic enzyme (GAME) genes, which encode key enzymes in SGA biosynthesis. Metabolomics analysis incorporating recombinant inbred lines generated from 95L368 and US28 yielded strong positive correlations between anthracnose resistance and accumulation of α-tomatine and several derivatives. Lastly, transient silencing of expression of the GAME genes GAME31 and GAME5 in anthracnose-susceptible tomato fruit yielded enhancements to anthracnose resistance. Together, our data support a role for SGAs in anthracnose defense in tomato, with a distinct SGA metabolomic profile conferring resistance to virulent Colletotrichum infections in ripe fruit.
炭疽病是一种广泛存在的植物病害，由多种真菌病原体炭疽菌引起。在茄科植物如番茄（Solanum lycopersicum）中，炭疽菌感染在发育中的果实中表现为静止、无症状状态，然后在成熟果实中转变为坏死性感染。通过对具有增强炭疽病抗性的番茄品系 95L368 的果实组织提取物进行分析，我们发现甾体糖苷生物碱（SGAs）在炭疽病抗性中发挥作用。与易感番茄品种 US28 的果实相比，SGAα-茄碱及其几种衍生物在 95L368 果实中的积累水平更高，并且 95L368 果实提取物对炭疽菌表现出抑菌活性。相应地，成熟和未成熟的 95L368 果实显示出糖基生物碱代谢酶（GAME）基因的表达增强，这些基因编码 SGA 生物合成中的关键酶。结合来自 95L368 和 US28 的重组自交系进行代谢组学分析，炭疽病抗性与α-茄碱和几种衍生物的积累之间存在强烈的正相关关系。最后，在易感炭疽病的番茄果实中瞬时沉默 GAME31 和 GAME5 GAME 基因的表达，可增强炭疽病抗性。总之，我们的数据支持 SGAs 在番茄炭疽病防御中的作用，具有独特的 SGA 代谢组学特征，赋予成熟果实对毒力炭疽菌感染的抗性。
