Adaptive significance and origin of flavonoid biosynthesis genes in the grain of cultivated cereals

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Abstract

The majority of cultivated cereals including maize, rice, wheat, barley, oat and rye are consisted of numerous varieties lacking anthocyanin pigmentation or having weak coloration of vegetative organs and/or caryopses. Only rare local races and wild related species have intense coloration of plants and/or grains. The coloration of caryopses is associated with the biosynthesis of colored flavonoids in maternal (pericarp and testa) and hybrid (aleuron) caryopsis tissues. The trait is controlled by dominant alleles of regulatory genes encoding conserved transcription factors of the MYB, bHLH-MYC, and WD40 families forming the MBW protein complex. Recent studies have proven the participation of uncolored and colored flavonoids in the response of plants to biotic and abiotic stresses, and significance of their presence in the whole grain foods has been determined. However, many questions about the adaptive effects and health benefits of anthocyanins remain unanswered. In particular, the reasons why the dominant alleles of regulatory genes controlling pericarp coloration did not become widespread in the course of domestication and breeding of cereals are not clear, although these genes receive special attention in association with health-improving effects of grain nutrition. This article discusses the similarity and specificity of the genetic control of the biosynthesis of flavonoids in the caryopsis in three related cultivated cereals – wheat, barley and rye, and their biological role in the development of the caryopsis and seed germination.

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About the authors

A. N. Bulanov

Saint Petersburg State University; Vavilov Institute of General genetics, Russian Academy of Sciences

Author for correspondence.
Email: an.bulanov20002014@gmail.com
Russian Federation, Saint Petersburg, 199034; Moscow, 119991

A. V. Voylokov

Vavilov Institute of General genetics, Russian Academy of Sciences

Email: av_voylokov@mail.ru
Russian Federation, Moscow, 119991

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2. Fig. 1. Scheme of the flavonoid biosynthesis pathway in plants. Classes of uncolored flavonoids are highlighted in shades of gray, colored flavonoids (phlobaphenes, proanthocyanidins, anthocyanidins, and anthocyanins) are highlighted in colors. The flavonoid biosynthesis pathway in plants begins, as with all phenolic compounds, with the successive transformations of phenylalanine catalyzed by phenylalanine ammonia-lyase (PAL), cinnamic acid 4-hydroxylase (C4H), and 4-coumarate-CoA ligase (4CL). Chalcone synthase (CHS) mediates the synthesis of naringenin-chalcone, the precursor of most flavonoids, and the combined action of chalcone synthase and chalcone reductase (CHR) causes the synthesis of chalcone, the precursor of the isoflavonoid isoliquirintigenin. Chalcones give rise to all classes of flavonoids, which is due to the work of the following enzymes: chalcone isomerase (CHI), flavone synthase 1 and 2, isoflavone synthase (IFS), flavanone-3-hydroxylase (F3H), flavonoid-3′- and –3′5′-hydroxylases (F3′H / F3′5′H, flavonoid-3′- / 3′5′-hydroxylase), flavonol synthase (FLS), dihydroflavonol reductase (DFR), leucoanthocyanidin reductase (LAR, leucoanthocyanidin reductase) and anthocyanidin reductase / leucoanthocyanidin dioxygenase (ANR, anthocyanidin reductase / LDOX, leucoanthocyanidin dioxygenase). Anthocyanins are synthesized by modifying anthocyanidins through methyltransferases (MT, methyltransferase), acyltransferases (AT, acyltransferase) and glycosyltransferases (GT, glycosyltransferase). Flavanones and dihydroflavonols can have different numbers of hydroxyl groups, which is mediated by the work of flavonoid-3′- and -3′5′-hydroxylases and subsequently leads to the synthesis of various phlobaphenes, flavones, flavonols, proanthocyanidins and anthocyanidins. Thus, cyanidin is characterized by the presence of a hydroxyl group in the 3'-position, and delphinidin – in both the 3'- and 5'-positions. The expression of various structural genes of flavonoid biosynthesis is directly activated by binding to their promoters of MBW complexes consisting of two dimerized molecules of the bHLH-MYC transcription factor, each associated with one molecule of the R2R3-MYB transcription factor. Such a complex is stabilized by the WD40 protein.

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