Arabidopsis Pollen Fertility Requires the Transcription Factors CIT1 and SPL7 that Regulate Copper Delivery to Anthers and Jasmonic Acid Synthesis

Corresponding author: Olena K. Vatamaniuk

A deficiency of the micronutrient (微量营养素) copper (Cu; 铜) leads to infertility (不育) and grain/seed yield reduction in plants. How Cu affects fertility, which reproductive structures require Cu, and which transcriptional networks coordinate Cu delivery to reproductive organs is poorly understood. Using RNA-seq analysis, we showed that the expression of a gene encoding a novel transcription factor, CITF1 (Cu-deficiency Induced Transcription Factor 1), was strongly upregulated in Arabidopsis thaliana flowers subjected to Cu deficiency. We demonstrated that CITF1 regulates Cu uptake into roots and delivery to flowers, and is required for normal plant growth under Cu deficiency. CITF1 acts together with a master regulator of copper homeostasis, SPL7 (Squamosa Promoter Binding Protein like7), and the function of both is required for Cu delivery to anthers and pollen fertility. We also found that Cu deficiency upregulates the expression of jasmonic acid (JA) biosynthetic genes in flowers, and increases endogenous JA accumulation in leaves. These effects are controlled in part by CITF1 and SPL7. Finally, we show that JA regulates CITF1 expression and that the JA biosynthetic mutant lacking the CITF1- and SPL7-regulated genes, LOX3 and LOX4, is sensitive to Cu deficiency. Together, our data show that CITF1 and SPL7 regulate Cu uptake and delivery to anthers, thereby influencing fertility, and highlight the relationship between Cu homeostasis, CITF1, SPL7, and the JA metabolic pathway.

微量营养素铜的缺陷会导致植物的不育和花粉、种子产量减产。铜如何影响植物育性，哪个生殖结构需要铜，哪个转录调控网络协调铜Cu传递到生殖器官还未得到很好的研究。利用RNA-seq分析，本文显示在缺铜的拟南芥中一个新的转录因子CITF1的表达受到强烈的上调。试验表明CITF1调控根对于Cu的吸收，传递到花，并且CITF1在缺铜条件下植物的正常生长是必须的。CITF1与一个调控Cu内稳态的蛋白SPL7共同作用，这两者的功能对于花药和花粉的育性都是必须的。作者还发现Cu缺失上调花中茉莉酸JA生物合成基因的表达，增加叶中内源JA的积累。这些影响部分由CITF1和SPL7控制。最终，本文试验显示JA调控CITF1基因的表达，JA生物合成突变体缺失了CITF1和SPL7的调控基因LOX3和LOX4，对于Cu缺失敏感。综上，本文的试验结果显示CITF1和SPL7调控Cu的吸收，并传递到花药，因此影响植物育性。

个人简介：乌克兰利沃夫州立大学，生物学，学士；乌克兰利沃夫州立大学、基辅国立大学，植物生理，博士；美国宾夕法尼亚大学，分子生物、生物化学、遗传学博士后；2005年，加入康奈尔大学；2011年，获终身教授。

doi: https://doi.org/10.1105/tpc.17.00363