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MAIZE GENETICS

Valuable allele in the wild

Science 365, 658–664 (2019).

Upright architecture with a small leaf angle represents an elite trait in maize that enables dense planting and yield increase. Although previous mutant analysis has uncovered two genes, lg1 and lg2, that control leaf angle, their mutant alleles cause phenotypes that are too severe to be useful in maize production. To understand the natural variations that regulate maize leaf angle, Jinge Tian and Chenglong Wang, from China Agricultural University, and colleagues cloned the causal genes underlying two quantitative trait loci (QTLs), UPRIGHT PLANT ARCHITECTURE 1 (UPA1) and UPA2, that confer upright architecture in maize.

Credit: Image courtesy of Feng Tian

The researchers used a segregating population derived from a cross between a maize inbred line and a teosinte accession. Among the 12 found QTLs, UPA1 and UPA2 displayed the largest phenotypic effects and were chosen for positional cloning.

UPA2 was mapped to a 240-base pair non-coding region 9.5 kb upstream of a B3-domain transcription factor gene, ZmRAVL1, and is a cis-element that regulates the expression of ZmRAVL1. The teosinte UPA2 allele confers a smaller leaf angle and is conducive to dense planting. Consistently, ZmRAVL1 positively regulates leaf angle, as disrupting this gene reduces leaf angle, while overexpressing this gene increases leaf angle. The causal variant of UPA2 was found to be a two-base sequence polymorphism that affects the binding of the DROOPING LEAF 1 (DRL1) protein. DRL1 interacts with the LIGULELESS 1 (LG1) protein, which binds to the promoter of ZmRAVL1 and activates its expression. So, the teosinte UPA2 allele indirectly regulates ZmRAVL1 expression via the DRL1–LG1–ZmRAVL1 module, which explains how the two-base causal variant regulates the expression of downstream ZmRAVL1.

The other QTL, UPA1, was mapped to a brassinosteroid C-6 oxidase (brd1) that converts 6-deoxocastasterone to castasterone, the immediate precursor of the hormone brassinolide. Unlike UPA2, the teosinte UPA1 allele confers a larger leaf angle. Mutant and transgenic analyses validated the function of brd1 in regulating maize leaf angle. Genetic and biochemical evidences suggest that the ZmRAVL1 protein binds to the promoter of brd1, activates brd1 transcription and positively regulates castasterone levels. So, UPA2–ZmRAVL1 modulates leaf angle by regulating brd1 and endogenous brassinosteroid content.

Although the teosinte UPA2 allele is present only in a minor proportion of teosinte accessions and was lost during maize domestication, field trials have shown that introducing this rare allele or a CRISPR-edited ZmRAVL1 allele into inbred or hybrid maize reduces leaf angle and enables dense planting as well as yield increase.

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Correspondence to Jun Lyu.

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Lyu, J. Valuable allele in the wild. Nat. Plants 5, 912 (2019). https://doi.org/10.1038/s41477-019-0521-x

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