Contributed by: Jongmin Nam
Pod corn (Zea mays var. tunicata) is a variety of maize that has kernels enclosed in elongated glumes (Figure 1), which is caused by a dominant gain-of-function mutation at the Tunicate (Tu) locus. The Tu also has a gene dosage effect, as there are several partial phenotypic revertants. Because the Tunicate phenotype is a universal characteristic of wild grasses and is different from naked kernels in maize varieties common today, pod corn is thought to be a progenitor of maize by some researchers. Despite long-standing interest in the evolution of this phenotype, molecular identity of the locus has remained unclear.
In a recent paper published in PNAS (1), Wingen et al. tested the hypothesis that genomic changes in a maize MADS-box transcription factor gene, ZMM19, are responsible for the Tunicate phenotype. They then obtained the following results that support the hypothesis: 1) The genomic location of ZMM19 is very close to the Tu locus; 2) Ectopic expression of ZMM19, a gene normally expressed only in vegetative tissues, in male and female inflorescence is observed in all pod corn lines tested; 3) Constitutive expression of ZMM19 in Arabidopsis resulted in enlarged sepals with unusual vegetative characters, which is similar to the Tunicate phenotype; 4) Insertions of a transposable element-like sequence in the 5' upstream region of the gene is observed, although the effect of this insertion has not been shown yet; 5) Perhaps most interestingly, the tandem duplication of ZMM19 specifically in pod corns and loss of one of the duplicates in several partial phenotypic revertant lines explain the gene dosage effect of the Tu. Moreover, this study suggests that pod corn is not a progenitor of common maize varieties, because the same insertion of transposable elements and gene duplication in the ZMM19 locus were not observed in wild grasses.
This study is a neat example of how a detailed molecular genetic study can help solving long-standing evolutionary questions, though in this case reciprocal engineering experiment of the ZMM19 locus between pod corn and common maize varieties is necessary to prove the authors' hypothesis.
In principle, any mutation has the potential to cause phenotypic evolution, and this is not the first study suggesting that gene expression change and gene copy number variation resulted in a phenotypic change. However, we still need more case studies to draw general principles of phenotype-mutation relationship, so I would never get tired of reading this type of paper.
The abstract of their paper is as follows.
Pod corn is a classic morphological mutant of maize in which the mature kernels of the cob are covered by glumes, in contrast to generally grown maize varieties in which kernels are naked. Pod corn, known since pre-Columbian times, is the result of a dominant gain-of-function mutation at the Tunicate (Tu) locus. Some classic articles of 20th century maize genetics reported that the mutant Tu locus is complex, but molecular details remained elusive. Here, we show that pod corn is caused by a cis-regulatory mutation and duplication of the ZMM19 MADS-box gene. Although the WT locus contains a single-copy gene that is expressed in vegetative organs only, mutation and duplication of ZMM19 in Tu lead to ectopic expression of the gene in the inflorescences, thus conferring vegetative traits to reproductive organs.
1. Wingen LU, Munster T, Faigl W, Deleu W, Sommer H, Saedler H, Theißen G. 2012. Molecular genetic basis of pod corn (Tunicate maize). Proceedings of the National Academy of Sciences of the United States of America 109: 7115-7120.