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Sequence variation, differential expression, and divergent evolution in starch-related genes among accessions of Arabidopsis thaliana

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Abstract

Transitory starch metabolism is a nonlinear and highly regulated process. It originated very early in the evolution of chloroplast-containing cells and is largely based on a mosaic of genes derived from either the eukaryotic host cell or the prokaryotic endosymbiont. Initially located in the cytoplasm, starch metabolism was rewired into plastids in Chloroplastida. Relocation was accompanied by gene duplications that occurred in most starch-related gene families and resulted in subfunctionalization of the respective gene products. Starch-related isozymes were then evolutionary conserved by constraints such as internal starch structure, posttranslational protein import into plastids and interactions with other starch-related proteins. 25 starch-related genes in 26 accessions of Arabidopsis thaliana were sequenced to assess intraspecific diversity, phylogenetic relationships, and modes of selection. Furthermore, sequences derived from additional 80 accessions that are publicly available were analyzed. Diversity varies significantly among the starch-related genes. Starch synthases and phosphorylases exhibit highest nucleotide diversities, while pyrophosphatases and debranching enzymes are most conserved. The gene trees are most compatible with a scenario of extensive recombination, perhaps in a Pleistocene refugium. Most genes are under purifying selection, but disruptive selection was inferred for a few genes/substitutiones. To study transcript levels, leaves were harvested throughout the light period. By quantifying the transcript levels and by analyzing the sequence of the respective accessions, we were able to estimate whether transcript levels are mainly determined by genetic (i.e., accession dependent) or physiological (i.e., time dependent) parameters. We also identified polymorphic sites that putatively affect pattern or the level of transcripts.

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Notes

  1. Note that SS sequence data for 26 accessions and transcript data for middle of the light period (MOL) for 6 accessions are taken from a previous study (Schwarte et al. 2013) and are included here to provide a comprehensive coverage of genes and transcripts underlying starch metabolism.

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Acknowledgments

The authors thank Thomas Altmann for providing plant seeds and Michael Lenhard for providing access to Realtime PCR equipment. Financial support by the Bundesministerium für Bildung und Forschung (BMBF) within the GoFORSYS initiative and by the University of Potsdam is gratefully acknowledged. MS thanks the Max Planck Institute of Molecular Plant Physiology, Potsdam-Golm, and the University of Guelph for generously permitting the use of the library. We would like to thank the anonymous reviewer for very useful comments and suggestions.

Conflict of interest

The authors declare that they have no conflict of interest.

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Author notes

  1. Fanny Wegner

    Present address: Division of Infection and Immunity, University College London, Cruciform Building, Gower Street, London, WC1E 6BT, UK

  2. Martin Steup

    Present address: Department of Molecular and Cellular Biology, University of Guelph, Guelph, ON, N1G 2W1, Canada

Authors and Affiliations

  1. Evolutionary Biology, Institute of Biochemistry and Biology, University of Potsdam, Karl-Liebknecht-Strasse 24-25, Building 26, 14476, Potsdam, Germany

    Sandra Schwarte, Fanny Wegner, Katja Havenstein & Ralph Tiedemann

  2. Bioinformatics, Institute of Biochemistry and Biology, University of Potsdam, Karl-Liebknecht-Strasse 24-25, Building 14, 14476, Potsdam, Germany

    Detlef Groth

  3. Plant Physiology, Institute of Biochemistry and Biology, University of Potsdam, Karl-Liebknecht-Strasse 24-25, Building 20, 14476, Potsdam, Germany

    Martin Steup

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  1. Sandra Schwarte
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Correspondence to Sandra Schwarte.

Electronic supplementary material

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11103_2015_293_MOESM1_ESM.pdf

Fig. S1 Duplications of chromosomal segments and the position of starch-related genes in the A. thaliana genome The chromosomes of A. thaliana (I to V) are shown as grey horizontal bars. The occurrence and positions of segmental duplications (similar sequences; various colors) were taken from Stein (2001; Fig. 3). Duplications occurred within and across chromosomes and could be either unidirectional or inverted (twisted bars). Chromosome length (given in megabases [Mb]) was modified according to TAIR 10.0. Starch-related genes are evenly distributed across the genome. The positions of the genes are given above each chromosome. (PDF 117 kb)

11103_2015_293_MOESM2_ESM.pdf

Fig. S2 Phylogenetic trees of the combined data set of A. thaliana. Rooted maximum likelihood trees among accessions of A. thaliana and A. lyrata as an outgroup based on gene sequences (including introns). The combined data set consists of 105 accessions comprising 26 accessions from our data set and 80 accessions from the 1001 Genome Project (Cao et al. 2011). Accessions that are used for Realtime PCR analyses are highlighted in the same color as in Figs. 3–8. (PDF 7940 kb)

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Schwarte, S., Wegner, F., Havenstein, K. et al. Sequence variation, differential expression, and divergent evolution in starch-related genes among accessions of Arabidopsis thaliana . Plant Mol Biol 87, 489–519 (2015). https://doi.org/10.1007/s11103-015-0293-2

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