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Structure, Evolution, and Expression of the Two Invertase Gene Families of Rice

Abstract

Invertases catalyze the irreversible hydrolysis of sucrose to glucose and fructose. Plants contain two unrelated families of these enzymes: acid forms that derive from periplasmic invertases of eubacteria and are found in cell wall and vacuole, and neutral/alkaline forms evolved from the cytosolic invertases of cyanobacteria. Genomes of rice (Oryza sativa) and thale cress (Arabidopsis thaliana) contain multiple genes encoding these two families. Here for rice we identify the member genes of a cell-wall group (designated OsCIN19), a vacuolar group (OsVIN12), and two ancient neutral/alkaline groups: α (OsNIN14) and β (OsNIN58). In Arabidopsis these groups contain six, two, four and five members, respectively. It is believed that the vacuolar group evolved from the cell-wall group. We provide evidence that the N-terminal signal peptide that directs cell-wall invertases co-translationally into the endoplasmic reticulum for secretion was replaced in the vacuolar group by a sequence similar to the complex N-terminal motif that targets alkaline phosphatase post-translationally to the vacuolar membrane of yeast. Since the last common ancestor of Arabidopsis and rice, the two invertase families evolved equally rapidly via gene duplication and gene loss, but the acid invertase family underwent ∼10 events of intron loss compared with a single event of intron gain in the neutral/alkaline invertase family. Transcripts were detected for all rice invertase genes except OsCIN9. The acid invertase genes showed greater spatial and temporal diversity of expression than the neutral/alkaline genes.

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Acknowledgments

We gratefully acknowledge financial support by grants from the German Federal Minister for Economic Cooperation and Development and the Swiss Development Coorporation. We thank project coordinators Dr. Renee Lafitte and Dr. Hei Leung. Dr. Arumugam Kathiresan and Dr. Kenneth McNally provided excellent technical advice. We thank Mr. Leonardo Estenor for assistance with plant growth and RNA extraction. Wim Van den Ende is a Postdoctoral Research Fellows of the Fund for Scientific Research-Flanders (Belgium) (FWO-Vlaanderen). Wim Van den Ende and André Van Laere are also supported by grants from KULeuven.

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Correspondence to John Bennett.

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Reviewing Editor: Dr. Rüdiger Cerff

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Ji, X., Van den Ende, W., Van Laere, A. et al. Structure, Evolution, and Expression of the Two Invertase Gene Families of Rice. J Mol Evol 60, 615–634 (2005). https://doi.org/10.1007/s00239-004-0242-1

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Keywords

  • Cell wall
  • Vacuole
  • Cytosol
  • Mitochondrion
  • Chloroplast
  • Oryza sativa
  • Arabidopsis thaliana
  • Subcellular targeting
  • Intron loss