ZmMADS69 functions as a flowering activator through the ZmRap2.7‐ZCN8 regulatory module and contributes to maize flowering time adaptation

Abstract

Summary Flowering time is a major determinant of the local adaptation of plants. Although numerous loci affecting flowering time have been mapped in maize, their underlying molecular mechanisms and roles in adaptation remain largely unknown. Here, we report the identification and characterization of MADS‐box transcription factor ZmMADS69 that functions as a flowering activator through the ZmRap2.7‐ZCN8 regulatory module and contributes to adaptation. We show that ZmMADS69 underlies a quantitative trait locus controlling the difference in flowering time between maize and its wild ancestor, teosinte. Maize ZmMADS69 allele is expressed at a higher level at floral transition and confers earlier flowering than the teosinte allele under long days and short days. Overexpression of ZmMADS69 causes early flowering, while a transposon insertion mutant of ZmMADS69 exhibits delayed flowering. ZmMADS69 shows pleiotropic effects for multiple traits of agronomic importance. ZmMADS69 functions upstream of the flowering repressor ZmRap2.7 to downregulate its expression, thereby relieving the repression of the florigen gene ZCN8 and causing early flowering. Population genetic analyses showed that ZmMADS69 was a target of selection and may have played an important role as maize spread from the tropics to temperate zones. Our findings provide important insights into the regulation and adaptation of flowering time.

Disentangling group specific QTL allele effects from genetic background epistasis using admixed individuals in GWAS: An application to maize flowering

“…Group-specific allele effects may also be due to an interaction with the genetic background. A first QTL matching this profile was detected by a SNP in the vicinity of Vgt3 on chromosome 3 [54,55] and its candidate gene ZmMADS69 [65]. This QTL showed an effect varying according to the genetic background: large in the dent, intermediate in the admixed and small in the flint.…”

“…), which supports the hypothesis of Vgt3 interacting with the genetic background. Recently, [65] demonstrated the action of ZmMADS69, the candidate gene of Vgt3, as being an activator of the regulatory module ZmRap2.7-ZCN8, which are the candidate genes of Vgt1 and Vgt2, respectively. The existence of such interactions is consistent with flowering time being controlled by a network of interacting loci, as now well established in model species arabidopis [67].…”

Interaction Between Induced and Natural Variation at oil yellow1 Delays Reproductive Maturity in Maize

“…In contrast, temperate maize germplasm is relatively day-neutral and flowering is primarily under the control of the autonomous pathway (Coles et al 2010). Mutant studies have identified loci critical to flowering in maize including: indeterminate1 (id1; Colasanti et al 1998); early phase change (epc; Vega et al 2002); delayed flowering1 (dlf1; Muszynski et al 2006); the cis-element polymorphism vegetative transitioning1 (vgt1; Salvi et al 2007) that regulates a downstream APETALA2-like transcription factor zmrap2.7; Zea mays mads4 (zmm4; Danilevskaya et al 2008); zmcct10 (Hung et al 2012); Zea mays centroradiales8 (zcn8; Meng et al 2011); Zea mays mads1 (zmmads1; Alter et al 2016); and Zea mays mads69 (zmmads69; Liang et al 2019). Many of these loci encode the maize orthologs of genes identified as regulators of flowering in Arabidopsis.…”

“…While this trait is convenient it is determined by both the days to floral transition of the meristem and the growth rate of the stem and emergence and maturation of floral structures. Nevertheless, many natural variants controlling days to reproductive maturity in maize map to bona fide flowering time loci identified by mutant studies including alleles of zmmads69, zmcct10, zcn8, dlf1, and vgt1 (Muszynski et al 2006;Salvi et al 2007;Meng et al 2011;Hung et al 2012;Guo et al 2018;Liang et al 2019).…”

Disentangling group specific QTL allele effects from genetic background epistasis using admixed individuals in GWAS: an application to maize flowering

“…Group-specific allele effects may also be due to an interaction with the genetic 508 background. A first QTL matching this profile was detected by a SNP in the vicinity of 509 Vgt3 on chromosome 3 [53,54] and its candidate gene ZmMADS69 [65]. This QTL 510 showed an effect varying according to the genetic background: large in the dent, 511 intermediate in the admixed and small in the flint.…”