SummaryFlooding is a widespread natural disaster that causes tremendous yield losses of global food production. Rice is the only cereal capable of growing in aquatic environments. Direct seeding by which seedlings grow underwater is an important cultivation method for reducing rice production cost. Hypoxic germination tolerance and root growth in waterlogged soil are key traits for rice adaptability to flooded environments. Alternative oxidase (AOX) is a non‐ATP‐producing terminal oxidase in the plant mitochondrial electron transport chain, but its role in hypoxia tolerance had been unclear. We have discovered that AOX1a is necessary and sufficient to promote germination/coleoptile elongation and root development in rice under flooding/hypoxia. Hypoxia enhances endogenous H2O2 accumulation, and H2O2 in turn activates an ensemble of regulatory genes including AOX1a to facilitate the conversion of deleterious reactive oxygen species to H2O2 in rice under hypoxia. We show that AOX1a and H2O2 act interdependently to coordinate three key downstream events, that is, glycolysis/fermentation for minimal ATP production, root aerenchyma development and lateral root emergence under hypoxia. Moreover, we reveal that ectopic AOX1a expression promotes vigorous root and plant growth, and increases grain yield under regular irrigation conditions. Our discoveries provide new insights into a unique sensor–second messenger pair in which AOX1a acts as the sensor perceiving low oxygen tension, while H2O2 accumulation serves as the second messenger triggering downstream root development in rice against hypoxia stress. This work also reveals AOX1a genetic manipulation and H2O2 pretreatment as potential targets for improving flooding tolerance in rice and other crops.

中文翻译：

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线粒体 AOX1a 和 H2O2 前馈信号环调节水稻的耐洪性


摘要洪水是一种广泛的自然灾害，它给全球粮食生产造成了巨大的产量损失。水稻是唯一能够在水生环境中生长的谷物。苗木在水下生长的直播是降低水稻生产成本的重要栽培方法。耐缺氧发芽和根系在涝积土壤中的生长是水稻适应洪水环境的关键性状。替代氧化酶 （AOX） 是植物线粒体电子传递链中一种不产生 ATP 的末端氧化酶，但其在缺氧耐受性中的作用尚不清楚。我们发现 AOX1a 对于在洪水/缺氧下促进水稻发芽/胚芽鞘伸长和根系发育是必要且足够的。缺氧增强了内源性 H2O2 积累，而 H2O2 反过来激活包括 AOX1a 在内的一系列调节基因，以促进缺氧下水稻中有害活性氧转化为 H2O2。我们表明 AOX1a 和 H 2 O 2 相互依赖地协调三个关键的下游事件，即糖酵解/发酵以最大限度地减少 ATP 产生、根通气组织发育和缺氧下的侧根出现。此外，我们揭示了异位 AOX1a 表达促进了根和植物的旺盛生长，并在常规灌溉条件下提高了谷物产量。我们的发现为独特的传感器-第二信使对提供了新的见解，其中 AOX1a 充当感知低氧张力的传感器，而 H 2 O 2 积累作为触发水稻下游根系发育的第二信使，以抵抗缺氧胁迫。这项工作还揭示了 AOX1a 基因操作和 H2O2 预处理是提高水稻和其他作物耐洪性的潜在靶点。