Control of Bird Feeding Behavior by Tannin1 through Modulating the Biosynthesis of Polyphenols and Fatty Acid-Derived Volatiles in Sorghum

First author: Peng Xie; Affiliations: CAS Institute of Genetics and Developmental Biology (中科院遗传与发育生物学研究所): Beijing, China

Corresponding author: Qi Xie

Bird predation during seed maturation causes great loss to agricultural production. In this study, through GWAS analysis of a large-scale sorghum germplasm diversity panel, we identified that Tannin1, which encodes a WD40 protein functioning in the WD40/MYB/bHLH complex, controls bird feeding behavior in sorghum. Metabolic profiling analysis showed that a group of sorghum accessions preferred by birds contain mutated tan1-a/b alleles and accumulate significantly lower levels of anthocyanins and condensed tannin compounds. In contrast, a variety of aromatic and fatty acid-derived volatiles accumulate at significantly higher levels in these bird-preference accessions. We subsequently conducted both sparrow feeding and sparrow volatile attractant assays, which confirmed, respectively, the antifeedant and attractant functions of these differentially accumulated metabolites. In addition, the connection between the biosynthesis pathway of anthocyanin and proanthocyanidin and the pathway of fatty acid–derived volatile biosynthesis was demonstrated by discovering that Tannin1 complex modulates fatty acid biosynthesis by regulating the expression of SbGL2 in sorghum, thus affecting the accumulation of fatty acid-derived volatiles. Taken together, our study identified Tannin1 as the gene underlying the major locus controlling bird feeding behavior in sorghum, illustrating an example of the identification of an ecologically impactful molecular mechanism from field observation and providing significant insights into the chemistry of bird–plant ecological interactions.

作物种子成熟期鸟类的捕食给农业生产造成了巨大的损失。本文中，作者通过对大范围高粱种质资源的全基因组关联分析GWAS鉴定到了一个作用于WD40/MYB/bHLH复合体的WD40蛋白编码基因Tannin1，该基因控制了鸟类对高粱种子的进食行为。代谢组分析显示受鸟类欢迎的一大类高粱材料含有突变了的tan1-a/b等位基因，这类高粱材料中积累的花青素和缩合单宁化合物较少。相反，芳香族和脂肪酸衍生的挥发物在这些鸟类偏好的高粱材料中显著高水平积累。随后，作者进行了麻雀投食和麻雀挥发物引诱剂试验，进一步证明了这两类差异积累的化合物各自对于鸟类的拒食和引诱作用。另外，作者发现Tannin1复合物通过调控高粱中SbGL2基因的表达调控脂肪酸生物合成，进而影响脂肪酸的挥发物的积累，从而揭示了花青素和原花青素生物合成通路与脂肪酸来源的挥发性化合物生物合成通路之间的关系。综上，本文的研究鉴定了Tannin1基因作为高粱中控制鸟类取食行为的主要位点，给出了一个从田间观察到生态影响分子机制鉴定的经典案例，同时也为鸟类-植物之间生态互作化学提供了全新的视野。

通讯：谢旗  (http://sourcedb.genetics.cas.cn/zw/zjrck/200907/t20090721_2130985.html)

个人简介：1987年，中山大学，学士；1990年，广东省微生物研究所，硕士；1994年，西班牙Universidad de Madrid大学，博士；1995-1998年，西班牙Universidad de Madrid、美国Rockefeller University，博士后。

研究方向：泛素蛋白酶体途径介导的蛋白修饰机制；植物与生物胁迫因子的相互作用及对非生物胁迫因子的响应及信号传导；高生物量植物甜高粱的分子设计。

doi: https://doi.org/10.1016/j.molp.2019.08.004

Journal: Molecular Plant

Published date: September 23, 2019