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The genomic signature of crop-wild introgression in maize.

Hufford MB, Lubinksy P, Pyhäjärvi T, Devengenzo MT, Ellstrand NC, Ross-Ibarra J - PLoS Genet. (2013)

Bottom Line: Through further characterization of these genomic regions and preliminary growth chamber experiments, we found evidence suggestive of the incorporation of adaptive mexicana alleles into maize during its expansion to the highlands of central Mexico.In contrast, very little evidence was found for adaptive introgression from maize to mexicana.Crop species, due to their exceptional genomic resources and frequent histories of spread into sympatry with relatives, should be particularly influential in these studies.

View Article: PubMed Central - PubMed

Affiliation: Department of Plant Sciences, University of California Davis, Davis, California, United States of America.

ABSTRACT
The evolutionary significance of hybridization and subsequent introgression has long been appreciated, but evaluation of the genome-wide effects of these phenomena has only recently become possible. Crop-wild study systems represent ideal opportunities to examine evolution through hybridization. For example, maize and the conspecific wild teosinte Zea mays ssp. mexicana (hereafter, mexicana) are known to hybridize in the fields of highland Mexico. Despite widespread evidence of gene flow, maize and mexicana maintain distinct morphologies and have done so in sympatry for thousands of years. Neither the genomic extent nor the evolutionary importance of introgression between these taxa is understood. In this study we assessed patterns of genome-wide introgression based on 39,029 single nucleotide polymorphisms genotyped in 189 individuals from nine sympatric maize-mexicana populations and reference allopatric populations. While portions of the maize and mexicana genomes appeared resistant to introgression (notably near known cross-incompatibility and domestication loci), we detected widespread evidence for introgression in both directions of gene flow. Through further characterization of these genomic regions and preliminary growth chamber experiments, we found evidence suggestive of the incorporation of adaptive mexicana alleles into maize during its expansion to the highlands of central Mexico. In contrast, very little evidence was found for adaptive introgression from maize to mexicana. The methods we have applied here can be replicated widely, and such analyses have the potential to greatly inform our understanding of evolution through introgressive hybridization. Crop species, due to their exceptional genomic resources and frequent histories of spread into sympatry with relatives, should be particularly influential in these studies.

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Growth chamber experiment.(A) Region of mexicana-to-maize introgression on chromosome 4 (indicated by blue hash on x-axis) shared across seven populations. Above: patterns of introgression seen in San Pedro (blue solid line) and Opopeo (blue dashed line) versus Puruandiro (red solid line) and Ixtlan (red dashed line). Below: pairwise FST of San Pedro/Opopeo (with introgression) versus Puruandiro/Ixtlan (without introgression). (B) Region of mexicana-to-maize introgression on chromosome 9 (indicated by blue hash on x-axis) shared across seven populations. Populations and comparisons are as in Figure 4A. (C) Five leaf sheaths from each of four maize populations grown under highland conditions. (D) Distribution of maize trait values (macrohairs, pigment extent and plant height at 50 days) from growth chamber experiment emulating highland conditions in populations with and without introgression.
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pgen-1003477-g004: Growth chamber experiment.(A) Region of mexicana-to-maize introgression on chromosome 4 (indicated by blue hash on x-axis) shared across seven populations. Above: patterns of introgression seen in San Pedro (blue solid line) and Opopeo (blue dashed line) versus Puruandiro (red solid line) and Ixtlan (red dashed line). Below: pairwise FST of San Pedro/Opopeo (with introgression) versus Puruandiro/Ixtlan (without introgression). (B) Region of mexicana-to-maize introgression on chromosome 9 (indicated by blue hash on x-axis) shared across seven populations. Populations and comparisons are as in Figure 4A. (C) Five leaf sheaths from each of four maize populations grown under highland conditions. (D) Distribution of maize trait values (macrohairs, pigment extent and plant height at 50 days) from growth chamber experiment emulating highland conditions in populations with and without introgression.

Mentions: Two of the shared introgressions that overlapped with QTL are of particular interest due to their previous characterization. One of these, on chromosome 4, overlaps with QTL for both pigment intensity and macrohairs [42], and maps to the same position as a recently identified putative inversion polymorphism showing significant differentiation between parviglumis and mexicana ([78]; Figure 4A). The second region, on chromosome 9, overlaps with a QTL for macrohairs [42] and includes the macrohairless1 (mhl1) locus [79] that promotes macrohair formation on the leaf blade and sheath of maize (Figure 4B). The two lowest elevation maize populations in our study (Puruandiro and Ixtlan) showed a conspicuous lack of introgression in these two genomic regions (Figure 4A and 4B). Analysis of pairwise differentiation (FST) between these populations and two populations showing fixed introgression in the two genomic regions (Opopeo and San Pedro; Figure 4A and 4B) revealed substantial differentiation: the region on chromosome 4 contained the only fixed SNP differences genome-wide (Puruandiro/Ixtlan versus Opopeo/San Pedro) and a SNP in the region on chromosome 9 was an extreme FST outlier. To explore the potential phenotypic effects of these genomic regions we conducted growth chamber experiments including ten maize plants from each of these four populations. Under temperature and day-length conditions typical of the highlands of Mexico (see Materials and Methods), the leaf sheaths of plants from populations where introgression was detected in the two genomic regions had 21-fold more macrohairs (t-test, p = 0.0002; Figure 4C and 4D), and showed greater pigmentation (t-test, p = 6E−06; Figure 4C and 4D). Introgressed plants were also ∼25 cm taller (t-test, p = 6E−06; Figure 4D), a finding consistent with adaptation to highland conditions and potentially associated with increased fitness. No significant difference in plant height was observed in a separate experiment under lowland conditions (t = test, p = 0.51), and a significant interaction was observed between introgression status and environmental treatment (ANOVA, F = 4.151, p = 0.045), with a disproportionate increase in plant height under lowland conditions in populations lacking introgression (Figure S7).


The genomic signature of crop-wild introgression in maize.

Hufford MB, Lubinksy P, Pyhäjärvi T, Devengenzo MT, Ellstrand NC, Ross-Ibarra J - PLoS Genet. (2013)

Growth chamber experiment.(A) Region of mexicana-to-maize introgression on chromosome 4 (indicated by blue hash on x-axis) shared across seven populations. Above: patterns of introgression seen in San Pedro (blue solid line) and Opopeo (blue dashed line) versus Puruandiro (red solid line) and Ixtlan (red dashed line). Below: pairwise FST of San Pedro/Opopeo (with introgression) versus Puruandiro/Ixtlan (without introgression). (B) Region of mexicana-to-maize introgression on chromosome 9 (indicated by blue hash on x-axis) shared across seven populations. Populations and comparisons are as in Figure 4A. (C) Five leaf sheaths from each of four maize populations grown under highland conditions. (D) Distribution of maize trait values (macrohairs, pigment extent and plant height at 50 days) from growth chamber experiment emulating highland conditions in populations with and without introgression.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3649989&req=5

pgen-1003477-g004: Growth chamber experiment.(A) Region of mexicana-to-maize introgression on chromosome 4 (indicated by blue hash on x-axis) shared across seven populations. Above: patterns of introgression seen in San Pedro (blue solid line) and Opopeo (blue dashed line) versus Puruandiro (red solid line) and Ixtlan (red dashed line). Below: pairwise FST of San Pedro/Opopeo (with introgression) versus Puruandiro/Ixtlan (without introgression). (B) Region of mexicana-to-maize introgression on chromosome 9 (indicated by blue hash on x-axis) shared across seven populations. Populations and comparisons are as in Figure 4A. (C) Five leaf sheaths from each of four maize populations grown under highland conditions. (D) Distribution of maize trait values (macrohairs, pigment extent and plant height at 50 days) from growth chamber experiment emulating highland conditions in populations with and without introgression.
Mentions: Two of the shared introgressions that overlapped with QTL are of particular interest due to their previous characterization. One of these, on chromosome 4, overlaps with QTL for both pigment intensity and macrohairs [42], and maps to the same position as a recently identified putative inversion polymorphism showing significant differentiation between parviglumis and mexicana ([78]; Figure 4A). The second region, on chromosome 9, overlaps with a QTL for macrohairs [42] and includes the macrohairless1 (mhl1) locus [79] that promotes macrohair formation on the leaf blade and sheath of maize (Figure 4B). The two lowest elevation maize populations in our study (Puruandiro and Ixtlan) showed a conspicuous lack of introgression in these two genomic regions (Figure 4A and 4B). Analysis of pairwise differentiation (FST) between these populations and two populations showing fixed introgression in the two genomic regions (Opopeo and San Pedro; Figure 4A and 4B) revealed substantial differentiation: the region on chromosome 4 contained the only fixed SNP differences genome-wide (Puruandiro/Ixtlan versus Opopeo/San Pedro) and a SNP in the region on chromosome 9 was an extreme FST outlier. To explore the potential phenotypic effects of these genomic regions we conducted growth chamber experiments including ten maize plants from each of these four populations. Under temperature and day-length conditions typical of the highlands of Mexico (see Materials and Methods), the leaf sheaths of plants from populations where introgression was detected in the two genomic regions had 21-fold more macrohairs (t-test, p = 0.0002; Figure 4C and 4D), and showed greater pigmentation (t-test, p = 6E−06; Figure 4C and 4D). Introgressed plants were also ∼25 cm taller (t-test, p = 6E−06; Figure 4D), a finding consistent with adaptation to highland conditions and potentially associated with increased fitness. No significant difference in plant height was observed in a separate experiment under lowland conditions (t = test, p = 0.51), and a significant interaction was observed between introgression status and environmental treatment (ANOVA, F = 4.151, p = 0.045), with a disproportionate increase in plant height under lowland conditions in populations lacking introgression (Figure S7).

Bottom Line: Through further characterization of these genomic regions and preliminary growth chamber experiments, we found evidence suggestive of the incorporation of adaptive mexicana alleles into maize during its expansion to the highlands of central Mexico.In contrast, very little evidence was found for adaptive introgression from maize to mexicana.Crop species, due to their exceptional genomic resources and frequent histories of spread into sympatry with relatives, should be particularly influential in these studies.

View Article: PubMed Central - PubMed

Affiliation: Department of Plant Sciences, University of California Davis, Davis, California, United States of America.

ABSTRACT
The evolutionary significance of hybridization and subsequent introgression has long been appreciated, but evaluation of the genome-wide effects of these phenomena has only recently become possible. Crop-wild study systems represent ideal opportunities to examine evolution through hybridization. For example, maize and the conspecific wild teosinte Zea mays ssp. mexicana (hereafter, mexicana) are known to hybridize in the fields of highland Mexico. Despite widespread evidence of gene flow, maize and mexicana maintain distinct morphologies and have done so in sympatry for thousands of years. Neither the genomic extent nor the evolutionary importance of introgression between these taxa is understood. In this study we assessed patterns of genome-wide introgression based on 39,029 single nucleotide polymorphisms genotyped in 189 individuals from nine sympatric maize-mexicana populations and reference allopatric populations. While portions of the maize and mexicana genomes appeared resistant to introgression (notably near known cross-incompatibility and domestication loci), we detected widespread evidence for introgression in both directions of gene flow. Through further characterization of these genomic regions and preliminary growth chamber experiments, we found evidence suggestive of the incorporation of adaptive mexicana alleles into maize during its expansion to the highlands of central Mexico. In contrast, very little evidence was found for adaptive introgression from maize to mexicana. The methods we have applied here can be replicated widely, and such analyses have the potential to greatly inform our understanding of evolution through introgressive hybridization. Crop species, due to their exceptional genomic resources and frequent histories of spread into sympatry with relatives, should be particularly influential in these studies.

Show MeSH
Related in: MedlinePlus