Uncovering the evolutionary origin of blue anthocyanins in cereal grains. (11th March 2020)

• Record Type: Journal Article
• Authors: Jia, Yong; Selva, Caterina; Zhang, Yujuan; Li, Bo; McFawn, Lee A.; Broughton, Sue; Zhang, Xiaoqi; Westcott, Sharon; Wang, Penghao; Tan, Cong; Angessa, Tefera; Xu, Yanhao; Whitford, Ryan; Li, Chengdao
• Is Part Of: Plant journal. Volume 101:Number 5(2020)
• Page Start: 1057
• Page End: 1074
• Publication Date: 2020-03-11
• Subjects: blue anthocyanin -- blue aleurone -- convergent evolution -- flavonoid 3′, 5′‐hydroxylase -- bHLH -- MYB; Plant molecular biology -- Periodicals; Plant cells and tissues -- Periodicals; Botany -- Periodicals; 580
• DOI: 10.1111/tpj.14557
• Languages: English
• ISSNs: 0960-7412

Abstract

Summary: Functional divergence after gene duplication plays a central role in plant evolution. Among cereals, only Hordeum vulgare (barley), Triticum aestivum (wheat) and Secale cereale (rye) accumulate delphinidin‐derived (blue) anthocyanins in the aleurone layer of grains, whereas Oryza sativa (rice), Zea mays (maize) and Sorghum bicolor (sorghum) do not. The underlying genetic basis for this natural occurrence remains elusive. Here, we mapped the barley Blx1 locus involved in blue aleurone to an approximately 1.13 Mb genetic interval on chromosome 4HL, thus identifying a trigenic cluster named MbHF35 (containing HvMYB4H, HvMYC4H and HvF35H ). Sequence and expression data supported the role of these genes in conferring blue‐coloured (blue aleurone) grains. Synteny analyses across monocot species showed that MbHF35 has only evolved within distinct Triticeae lineages, as a result of dispersed gene duplication. Phylogeny analyses revealed a shared evolution pattern for MbHF35 in Triticeae, suggesting that these genes have co‐evolved together. We also identified a Pooideae‐specific flavonoid 3′, 5′‐hydroxylase (F3′5′H) lineage, termed here Mo_F35H2, which has a higher amino acid similarity with eudicot F3′5′Hs, demonstrating a scenario of convergent evolution. Indeed, selection tests identified 13 amino acid residues in Mo_F35H2 that underwent positive selection, possibly driven by protein thermostablility selection. Furthermore, through the interrogation of barley germplasm there is evidence that HvMYB4H and HvMYC4H have undergone human selection. Collectively, our study favours blue aleurone as a recently evolved trait resulting from environmental adaptation. Our findings provide an evolutionary explanation for the absence of blue anthocyanins in other cereals and highlight the importance of gene functional divergence for plant diversity and environmental adaptation. Significance Statement: Our findings provide a genetic and evolutionary explanation of why only barley, wheat and rye grains can develop a blue anthocyanins in nature, but not rice, maize and sorghum.