The Role of Regulatory Genes during Maize Domestication: Evidence from Nucleotide Polymorphism and Gene Expression

By Zhao, Qiong; Thuillet, Anne-Céline et al. | Genetics, April 2008 | Go to article overview

The Role of Regulatory Genes during Maize Domestication: Evidence from Nucleotide Polymorphism and Gene Expression


Zhao, Qiong, Thuillet, Anne-Céline, Uhlmann, Nathan K., Weber, Allison, Rafalski, J. Antoni, Allen, Stephen M., Tingey, Scott, Doebley, John, Genetics


ABSTRACT

We investigated DNA sequence variation in 72 candidate genes in maize landraces and the wild ancestor of maize, teosinte. The candidate genes were chosen because they exhibit very low sequence diversity among maize inbreds and have sequence homology to known regulatory genes. We observed signatures of selection in 17 candidate genes, indicating that they were potential targets of artificial selection during domestication. In addition, 21 candidate genes were identified as potential targets of natural selection in teosinte. A comparison of the proportion of selected genes between our regulatory genes and genes unfiltered for their potential function (but also with very low sequence diversity among maize inbreds) provided some weak evidence that regulatory genes are overrepresented among selected genes. We detected no significant association between the positions of genes identified as potential targets of selection during domestication and quantitative trait loci (QTL) responsible for maize domestication traits. However, a subset of these genes, those identified by sequence homology as kinase/phosphatase genes, significantly cluster with the domestication QTL. We also analyzed expression profiles of genes in distinct maize tissues and observed that domestication genes are expressed on average at a significantly higher level than neutral genes in reproductive organs, including kernels.

REGULATORY genes play an important role in development by controlling the expression of downstream structural or regulatory genes. It has been suggested that changes in function or expression of regulatory genes may be associated with the diversification of plant morphology (DOEBLEY and LUKENS 1998; PURUGGANAN 1998, 2000). Two regulatory genes controlling differences in plantmorphology betweenmaize and teosinte, teosinte branched1 (tb1) and teosinte glume architecture1 (tga1), have been identified through quantitative trait locus (QTL) mapping (DOEBLEY et al. 1997; WANG et al. 2005). Both of these regulatory genes are responsible for major morphology changes that occurred during thedomestication ofmaize. An increase in the expression of tb1 led to reduced branching in maize (DOEBLEY et al. 1997), whereas a change in the function of the tga1 proteinappears tobe responsible for reducing the size of the casing around the kernel in teosinte (WANG et al. 2005). In other crops, genes that control domestication traits were also revealed to encode regulatory genes, including the tomato gene fw2.2 affecting fruit weight (FRARY et al. 2000), the rice shattering gene (LI et al. 2006), and the Q gene in wheat (SIMONS et al. 2006). This list suggests that regulatory genes may have been important targets of selection during crop domestication.

To identify other maize genes that were targets of selection during domestication, approaches based on molecular population genetics have been employed (WRIGHT and GAUT 2005). Evidence of selection can be detected either by standard tests of the neutral equilibrium model or by a coalescence-simulation (CS)- based test. The coalescence-simulation-based test assays whether the relative loss of nucleotide diversity in maize as compared to teosinte is too large to be accounted for by a domestication bottleneck alone such that selection can be inferred. The Hudson-Kreitman-Aguadé (HKA) test, a standard neutrality test, assays whether the amount of nucleotide diversity in the gene of interest is significantly lower than the amount of nucleotide diversity in neutral genes in maize. Application of these tests provided evidence that the domestication genes tb1 and tga1 were both targets of selection during domestication (WANG et al. 1999, 2005; CLARK et al. 2004).

Recently, large-scale genomic screens using molecular population genetics methods have identified a long list of genes that were possible targets of selection during maize domestication (VIGOUROUX et al. 2002; WRIGHT et al. 2005; YAMASAKI et al.

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The Role of Regulatory Genes during Maize Domestication: Evidence from Nucleotide Polymorphism and Gene Expression
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