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Parallel evolution of storage roots in morning glories (Convolvulaceae)

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Eserman, Lauren A., Jarret, Robert L., Leebens-Mack, James H.·2018·BMC Plant Biology
DOI 10.1186/s12870-018-1307-4PMC PMC5975488
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Abstract

BACKGROUND: Storage roots are an ecologically and agriculturally important plant trait that have evolved numerous times in angiosperms. Storage roots primarily function to store carbohydrates underground as reserves for perennial species. In morning glories, storage roots are well characterized in the crop species sweetpotato, where starch accumulates in storage roots. This starch-storage tissue proliferates, and roots thicken to accommodate the additional tissue. In morning glories, storage roots have evolved numerous times. The primary goal of this study is to understand whether this was through parallel evolution, where species use a common genetic mechanism to achieve storage root formation, or through convergent evolution, where storage roots in distantly related species are formed using a different set of genes. Pairs of species where one forms storage roots and the other does not were sampled from two tribes in the morning glory family, the Ipomoeeae and Merremieae. Root anatomy in storage roots and fine roots was examined. Furthermore, we sequenced total mRNA from storage roots and fine roots in these species and analyzed differential gene expression. RESULTS: Anatomical results reveal that storage roots of species in the Ipomoeeae tribe, such as sweetpotato, accumulate starch similar to species in the Merremieae tribe but differ in vascular tissue organization. In both storage root forming species, more genes were found to be upregulated in storage roots compared to fine roots. Further, we find that fifty-seven orthologous genes were differentially expressed between storage roots and fine roots in both storage root forming species. These genes are primarily involved in starch biosynthesis, regulation of starch biosynthesis, and transcription factor activity. CONCLUSIONS: Taken together, these results demonstrate that storage roots of species from both morning glory tribes are anatomically different but utilize a common core set of genes in storage root formation. This is consistent with a pattern of parallel evolution, thus highlighting the importance of examining anatomy together with gene expression to understand the evolutionary origins of ecologically and economically important plant traits.

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Fig. 1 Root cross sections from three pairs of species, where one member of the species pair forms storage roots and the other does not. To the left is a phylogeny depicting the evolutionary relationships among the six species with arrows denoting the two tribes, Ipomoeeae and Merremieae. The left-most three columns are root sections stained with Lugol’s iodine, which indicates starch a dark blue to black color. The right-most three columns are root sections stained with phloroglucinol-HCl, which stains lignin orange to pink. Scale bars are included with each section. Black bars are 1 mm, and blue bars are 0.5 mm in length. White arrows indicate starch-storage tissue
Fig. 1 Root cross sections from three pairs of species, where one member of the species pair forms storage roots and the other does not. To the left is a phylogeny depicting the evolutionary relationships among the six species with arrows denoting the two tribes, Ipomoeeae and Merremieae. The left-most three columns are root sections stained with Lugol’s iodine, which indicates starch a dark blue to black color. The right-most three columns are root sections stained with phloroglucinol-HCl, which stains lignin orange to pink. Scale bars are included with each section. Black bars are 1 mm, and blue bars are 0.5 mm in length. White arrows indicate starch-storage tissueCC BY · PubMed Central
Fig. 2 Heat map of genes differentially expressed between storage roots and fine roots of sweet potato, Ipomoea batatas (a) and Distimake dissectus (b). Each row in the heatmap is depicting the expression patterns of each transcript, and each column represents each library. A dendrogram illustrating clustering of libraries is shown above each heatmap, and a dendrogram showing clustering of transcript expression patterns is to the left of each heatmap. c Number of transcripts differentially expressed between storage and fine roots and the number that were orthologous between I. batatas and D. dissectus
Fig. 2 Heat map of genes differentially expressed between storage roots and fine roots of sweet potato, Ipomoea batatas (a) and Distimake dissectus (b). Each row in the heatmap is depicting the expression patterns of each transcript, and each column represents each library. A dendrogram illustrating clustering of libraries is shown above each heatmap, and a dendrogram showing clustering of transcript expression patterns is to the left of each heatmap. c Number of transcripts differentially expressed between storage and fine roots and the number that were orthologous between I. batatas and D. dissectusCC BY · PubMed Central
Fig. 3 Starch biosynthetic pathway adapted from Bahaji et al. 2014. Metabolites are shown in black, and enzymes are shown in green. Shown are TMM-normalized FPKM values for homologs in all four species (bata = Ipomoea batatas, trif = I. trifida, diss = Distimake dissectus, and quin = D. quinquefolius). Grey boxes indicate genes where orthology could not be determined. Stacked boxes indicate homologs of a particular gene. Gene names with an asterisk were found to be significantly differentially expressed at a FDR < 0.05 in both I. batatas and D. dissectus. The heatmap is colored by percentile, where genes in the 10th percentile were colored yellow and those in the 90th percentile were colored dark blue
Fig. 3 Starch biosynthetic pathway adapted from Bahaji et al. 2014. Metabolites are shown in black, and enzymes are shown in green. Shown are TMM-normalized FPKM values for homologs in all four species (bata = Ipomoea batatas, trif = I. trifida, diss = Distimake dissectus, and quin = D. quinquefolius). Grey boxes indicate genes where orthology could not be determined. Stacked boxes indicate homologs of a particular gene. Gene names with an asterisk were found to be significantly differentially expressed at a FDR < 0.05 in both I. batatas and D. dissectus. The heatmap is colored by percentile, where genes in the 10th percentile were colored yellow and those in the 90th percentile were colored dark blueCC BY · PubMed Central
Fig. 4 Mean TMM-normalized FPKM values for the seven transcription factors found to be significantly differentially expressed between storage and fine roots in both Ipomoea batatas and Distimake dissectus at a FDR < 0.05. The heatmap depicts mean TMM-normalized FPKM values for orthologs of the transcription factors in each tissue type for all four species (bata = Ipomoea batatas, trif = I. trifida, diss = Distimake dissectus, and quin = D. quinquefolius). The heatmap was colored by percentile, where genes in the 10th percentile were colored yellow and those in the 90th percentile were colored dark blue. No ortholog of KN1 could be identified in the transcriptome assembly of I. trifida, and no ortholog of HAT22 could be identified in D. quinquefolius
Fig. 4 Mean TMM-normalized FPKM values for the seven transcription factors found to be significantly differentially expressed between storage and fine roots in both Ipomoea batatas and Distimake dissectus at a FDR < 0.05. The heatmap depicts mean TMM-normalized FPKM values for orthologs of the transcription factors in each tissue type for all four species (bata = Ipomoea batatas, trif = I. trifida, diss = Distimake dissectus, and quin = D. quinquefolius). The heatmap was colored by percentile, where genes in the 10th percentile were colored yellow and those in the 90th percentile were colored dark blue. No ortholog of KN1 could be identified in the transcriptome assembly of I. trifida, and no ortholog of HAT22 could be identified in D. quinquefoliusCC BY · PubMed Central

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Metadata

Authors
Eserman, L. A., Jarret, R. L., & Leebens-Mack, J. H.
Affiliations
  • University of Georgia (US)
  • United States Department of Agriculture (US)
Corresponding author
Eserman, Lauren A.
ORCID
Venue
BMC Plant Biology
Publisher
Springer Science and Business Media LLC
Published
2018-05-29
Volume
18
Issue
1
Pages
95-95
ISSN
1471-2229 (ISSN-L)
DOI
10.1186/s12870-018-1307-4
PMC
PMC5975488
OpenAlex
W2807384079
Cited by
25
References
55
Citations by year
2026: 4 · 2024: 4 · 2023: 2 · 2022: 4 · 2021: 6 · 2020: 2 · 2019: 3
FWCI
2.43
Type
journal article
Language
en
Open access
Licence
Locations
  • BMC Plant Biology (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • USDA
  • Society for the Study of Evolution
  • UGA Plant Biology Department
  • Society for Integrative and Comparative Biology
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Parasitism and Resistance
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant nutrient uptake and metabolism
Keywords
tuberous roots, parallel evolution, convergent evolution, Convolvulaceae, Ipomoea batatas, starch biosynthesis, root anatomy, fine roots, differential gene expression, orthologs, transcription factors, carbohydrate storage
MeSH terms
Phenotype, RNA, Messenger, Starch, Up-Regulation, Gene Expression Regulation, Plant, Plant Roots, Evolution, Molecular, Gene Expression Profiling, Ipomoea batatas, Ipomoea, Biosynthetic Pathways, Transcriptome

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Eserman, L. A., Jarret, R. L., & Leebens-Mack, J. H. (2018). Parallel evolution of storage roots in morning glories (Convolvulaceae). BMC Plant Biology. https://doi.org/10.1186/s12870-018-1307-4