Published online 1 November 2006
Published in Crop Sci 46:S-49-S-54 (2006)
© 2006 Crop Science Society of America
677 S. Segoe Rd., Madison, WI 53711 USA
ORIGINAL RESEARCH
Recurrent Mutation and Genome Evolution: Example of Sugary1 and the Origin of Sweet Maize
William F. Tracy*,
Sherry R. Whitt and
Edward S. Buckler
W.F. Tracy, Dep. of Agronomy, Univ. of Wisconsin, Madison, WI 53706, USA; S.R. Whitt, Raleigh, NC 27695, USA (formerly) USDA-ARS, BASF-Plant Science, RTP, NC 22709, USA (currently); E.S. Buckler, USDA-ARS, Dep. of Plant Breeding & Genetics, Cornell Univ., Ithaca, NY 14853, USA
* Corresponding author (wftracy{at}wisc.edu).
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ABSTRACT
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In maize (Zea mays L.), mutations at the Sugary 1 locus are the genetic bases for maize with specialty uses cultivated throughout the western hemisphere precontact (pre-Columbian). The traditional North American sweet maize is homozygous for a recessive sugary1 (su1) allele. Determining the number of unique alleles among su1 maize races is relevant to the debate in archeology and evolutionary biology over whether independent mutation or migration plays a dominant role in the spread of novel phenotypes. We sequenced su1 from 57 cultivars of su1 maize and determined that five independent mutations have been selected. Three of these five alleles were single base pair changes at highly conserved sites and a fourth was a 1.3-kbp transposon. It will be interesting to note if future study in a variety of disciplines will lead to consensus on the significant role of recurrent mutation in evolution.
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INTRODUCTION
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"SEX IS GOOD, but not as good as fresh sweet corn." When American humorist Garrison Keillor made this now famous remark he probably was not aware that his indebtedness is owed to a recessive allele at Sugary 1 (su1). Maize homozygous for recessive su1 has been cultivated in much of the maize growing region of the western hemisphere since precontact times (Wellhausen et al., 1952; Grobman et al., 1961). The gene is now known to code for an isoamylase functioning in starch synthesis in maize endosperm (Rahman et al., 1998; Dinges et al., 2001). Recessive su1 results in the accumulation of phytoglycogen rather than starch (Marshall and Tracy, 2003). Phytoglycogen, a highly branched water soluble polysaccharide, gives sweet maize its creamy texture (Marshall and Tracy, 2003).
In 1890 Willet M. Hays (1890, p. 89–90) anticipated Mendel's laws by reporting the phenomena of dominance, recessiveness, segregation, and independent assortment by clearly describing the 3:1 segregation ratio in controlled crosses of flint maize and su1 maize. Alleles at Su1 were among the first to be genetically characterized by Correns (1901) following the rediscovery of Mendel. While su1 was one of the earliest genes genetically characterized in maize, maize geneticists have long debated its origins. The controversy has centered on whether one or two independent mutations at Su1 have been selected and fixed. Galinat (1971) and Mangelsdorf (1974) used morphological evidence to argue that the su1 allele was selected once in the Peruvian Andes and then introgressed into local maize throughout the hemisphere. In this hypothesis (Mangelsdorf, 1974), the Peruvian race Chullpi was the original su1 source and the progenitor of the race Maiz Dulce from Jalisco, Mexico. Maize Dulce, in turn, was crossed to popcorn Reventador to produce Ducillo del Noroeste in northwest Mexico (Wellhausen et al., 1952). From Ducillo del Noroeste, su1 was introgressed into northern races including Northern Flint, the progenitor of modern commercial sweet corn (Revilla and Tracy, 1995).
Others counter that independent mutations at su1 were fixed twice—first, thousands of years ago in the Andes, and again more recently in what is now the northeastern USA (Erwin, 1934, 1947, 1951). This theory is based on three main arguments: (i) lack of sweet maize in archeological collections from eastern North America, (ii) observations of spontaneous mutations to the su1 allele in field maize, and (iii) the fact that no written record of sweet maize exists in the USA until the nineteenth century. The earliest written English references to what is indisputably su1 corn, based on its distinctive wrinkled seed, appeared in 1801 in a book called Bordley's Husbandry (Sturtevant, 1972) and 1810 in Thomas Jefferson's Garden Book (Huelson, 1954). Thus, the dispute over the origins of su1 maize fuels the larger debate in archeology and evolutionary biology over whether independent mutation or migration plays a more dominant role in the spread of novel phenotypes.
To help resolve this controversy, we sequenced the Su1 gene from 57 accessions of su1 maize and compared the results with normal Su1 alleles identified in a previous study (Whitt et al., 2002) (Fig. 1A
and Table 1).
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Fig. 1. Distribution of su1 alleles. Alleles are color coded based on (C). (A) The geographic distribution of su1 mutant alleles. Mixed accessions are indicated by split circles. Exact geographic locations for the majority of the northeastern U.S. accessions are unknown. (B) The three su1 amino acid changes projected on Pseudomonas isoamylase crystal structure (Katsuya et al., 1998). (C) Structure of the Su1 gene and position of mutations. A fifth allele, from the Peruvian accessions, is not depicted in this figure.
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Materials and Methods
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Seed from 57 sugary1 accessions encompassing six geographic areas in the USA, Mexico, and Peru were obtained from the North Central Plant Introduction Center in Ames, IA, and the University of Wisconsin sweet corn breeding program (Table 1). Seed were germinated and leaf tissue harvested from two plants per accession at 14 d. DNA was extracted in a 96-well format from frozen tissue. Samples were PCR amplified and sequenced at the SU1 locus. Two 1000-bp regions of the gene with previously identified sweet mutations, an exon 1 transposable element found in a sample from Jalisco, Mexico (Whitt et al., 2002), and a tryptophan to arginine substitution at residue 578 in northeastern U.S. sweet corn (Dinges et al., 2001; Whitt et al., 2002) were initially examined.
Nucleotide alignments were generated using Biolign alignment software (Thomas Hall, 2000, North Carolina State University). Twenty-nine accessions of nonsweet maize were included in the alignments to enable detection of polymorphisms unique to sweet maize. Representative accessions from each region demonstrating a novel mutation were PCR amplified and sequenced for the entire SU1 locus. The accessions sequenced were PI 474214 (Ducillo de Noroeste, Sonora, Mexico), WI:93:943 (‘Mandan Red’), and PI 213796 (‘Nueta’, northcentral USA), and WI:94:4430 (‘Hopi White’, southwestern USA). No additional polymorphisms were discovered in a nucleotide alignment of the 11 kbp su1 gene when compared with 32 completely sequenced maize inbred lines.
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Results and Discussion
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Our survey revealed five independent origins in the history of sweet maize, four of which were identified to the nucleotide level (Fig. 1C, Table 1). All 35 of the northeastern USA cultivars we sequenced had a tryptophan to arginine substitution at residue 578 (W578R). These are the progenitors of modern commercial sweet maize (Revilla and Tracy, 1995; Gerdes and Tracy, 1994). The four cultivars of unknown race and geographic origin also had the W578R allele. These results are similar to those reported by Whitt et al. (2002), and this W578R allele was also one of two identified by Dinges et al. (2001).
Three Ducillo de Noroestes accessions from northwest Mexico and five of the seven accessions from southwestern USA had an asparagine 561 to serine mutation (N561S), indicating a second event. The two remaining southwestern USA accessions carried the W578R allele. This finding may represent the origin of this allele in what is now Arizona or New Mexico, or perhaps signal a more recent immigration of the allele to this area.
A third independent event was confirmed by the 1.3-kbp transposable element in exon 1 found in Maiz Dulce accession from Guanajuato, Mexico (PI 628428). This is the same transposable element previously observed in Mexican su1 maize (Whitt et al., 2002). The other Maiz Dulce accession (PI 503576) segregated for both the transposable element and the N561S alleles. PI 503576 may be a derived from a cross between a Maiz Dulce and a Ducillo de Noroeste. PI 503576 has morphological resemblance to Maiz Dulce, but was collected in a region more typical of the adaptive zone for Ducillo de Noroeste (www.ars-grin.gov, verified 26 May 2006). PI 503576 was collected at an altitude of 190 m in northern Sinaloa (26°25' N, 108°31' W), less than 100 km from where one of the Ducillo de Noroeste accessions (PI 474214) was collected in the state of Sonora (27° N, 109° W). The relatively low altitude at which PI 503576 grows is more typical of Ducillo de Noroeste than the midaltitude adapted Maiz Dulce (1000–1500 m).
A fourth event most likely occurred in northcentral USA. Three of the four accessions believed to be from this region were characterized by an arginine to cysteine mutation at residue 504 (R504C), with the fourth (Hidatsa) possessing the W578R allele. Two of the three accessions were heterozygous for W578R and R504C.
Finally, despite sequencing 12 kb of Su1 in two Chullpi accessions from the Andes, we were unable to identify a mutation that causes the su1 phenotype. However, as the four alleles described above were not present, a fifth independent origin is apparent. Complementation tests demonstrate that the glassy wrinkled endosperm of Chullpi is due to an allele at su1.
Of the five mutation events, the three single amino acid substitutions are found in highly conserved residues. A comparison of the 25 isoamlyases among plants, archaea, and eubacteria revealed that residue 504 is conserved in 92% of the homologs, residue 561 in 100%, and residue 578 in 84% (Fig. 2
). Interestingly, all three residues reside within a single cleft of the enzyme, away from the centrally embedded active site (Fig. 1B).
With at least five independent mutations selected and fixed by agriculturalists in American sugary maize, the multiple origins of su1 provide a clear example of the importance of reinvention in the evolution of unique crops. This stands in sharp contrast to the emphasis previously placed on long range migrations to explain the presence of sweet maize across the Americas. Both historical and archeological studies support the idea that the Chullpi allele, the Maiz Dulce allele from central Mexico containing the 1.3-kbp transposon, and the N561S allele from northwestern Mexico/southwestern USA occurred precontact. Most probably, the northcentral R504C allele originated in the northern Great Plains sometime after maize was introduced into that region. While it is likely the northeastern W578R allele was selected in the northeastern USA between 200 and 300 yr ago, it could have originated in either the northcentral or southwestern regions and migrated to the northeast.
These su1 alleles have a major phenotypic effect that is easily identifiable by humans. It will be interesting to learn if future investigation confirms the role of recurrent mutation in evolution occurs primarily when alleles have a very large phenotypic effect, as well as whether or not the role of recurrent mutation in crop evolution and domestication is currently underestimated.
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ACKNOWLEDGMENTS
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We thank US NSF (DBI-0321467) and the College of Agricultural and Life Sciences, University of Wisconsin–Madison for supporting this research, Natalie Stevens for technical editing, and Jim Coors, Irwin Goldman, and Shawn Kaeppler for their assistance in preparing the manuscript.
Received for publication March 4, 2006.
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ABSTRACT
INTRODUCTION
