Striped stem borer (SSB) is one of the most damaging pests in rice production worldwide. Previously, we preliminarily demonstrated that indica rice Jiazhe LM, an OsT5H (encoding tryptamine-5-hydroxylase) knockout mutant deficient in serotonin, had increased resistance to SSB as compared with its wildtype parent Jiazhe B. However, the full scenario of SSB resistance and the underlying mechanism remain unknown. In this study, we first demonstrated that the OsT5H knockout could generally increase rice resistance to SSB and then proved that the OsT5H knockout does not disrupt the innate defense response of rice plants to SSB infestation, that is, OsT5H knockout mutations neither had significant effect on the transcriptional response of defense genes upon SSB infestation, nor the profile of defense related metabolites and plant hormones, such as lignin, salicylic acid, jasmonic acid, and abscisic acid, nor the activity of reactive oxygen species (ROS) scavenging enzymes and the ROS contents. We then demonstrated that supplementation of serotonin promoted SSB growth and performance in artificial diet feeding experiments. We observed that SSB larvae feeding on Jiazhe B had serotonin 1.72- to 2.30-fold that of those feeding on Jiazhe LM at the whole body level, and more than 3.31 and 1.84 times in the hemolymph and head, respectively. Further studies showed that the expression of genes involved in serotonin biosynthesis and transport was ~88.1% greater in SSB larvae feeding on Jiahze LM than those feeding on Jiazhe B. These observations indicated that SSB increases serotonin synthesis when feeding on serotonin deficient rice but is unable to fully compensate the dietary serotonin deficiency. Put together, the present study strongly suggests that it is the deficiency of serotonin, not the secondary effect of OsT5H knockout on innate defense response confers the SSB resistance in rice, which implies that reducing serotonin level, particularly through inhibition of its inductive synthesis upon SSB damage, could be an efficient strategy for breeding SSB resistant varieties.

中文翻译：

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破坏血清素生物合成可增加对条纹二化螟的抗性，而不改变水稻的先天防御反应

条纹二化螟 (SSB) 是全球水稻生产中最具破坏性的害虫之一。此前，我们初步证明籼稻嘉哲LM是一种缺乏血清素的OsT5H（编码色胺5-羟化酶）敲除突变体，与其野生型亲本嘉哲B相比，其对SSB的抗性有所增强。然而，SSB抗性的完整情况和根本机制仍不清楚。在本研究中，我们首先证明了OsT5H敲除通常可以提高水稻对SSB的抗性，然后证明OsT5H敲除不会破坏水稻植物对SSB侵染的先天防御反应，即OsT5H敲除突变对水稻对SSB侵染的先天防御反应没有显着影响。防御基因对 SSB 侵染的转录反应，也不是防御相关代谢物和植物激素（例如木质素、水杨酸、茉莉酸和脱落酸）的概况，也不是活性氧 (ROS) 清除酶和 ROS 的活性内容。然后，我们在人工饲料喂养实验中证明，补充血清素可促进 SSB 的生长和性能。我们观察到，取食嘉蛰B的SSB幼虫全身血清素含量是取食嘉蛰LM的幼虫的1.72至2.30倍，血淋巴和头部的血清素含量分别是其3.31和1.84倍。进一以充分补偿饮食中血清素的缺乏。总而言之，本研究强烈表明，正是血清素的缺乏，而不是OsT5H敲除对先天防御反应的二次影响，赋予了水稻 SSB 抗性，这意味着降低血清素水平，特别是通过抑制其对 SSB 的诱导合成损害，可能是培育 SSB 抗性品种的有效策略。