Insights into Regulation of C2 and C4 Photosynthesis in Amaranthaceae/ Chenopodiaceae Using RNA-Seq

Int J Mol Sci. 2021 Nov 9;22(22):12120. doi: 10.3390/ijms222212120.

Abstract

Amaranthaceae (incl. Chenopodiaceae) shows an immense diversity of C4 syndromes. More than 15 independent origins of C4 photosynthesis, and the largest number of C4 species in eudicots signify the importance of this angiosperm lineage in C4 evolution. Here, we conduct RNA-Seq followed by comparative transcriptome analysis of three species from Camphorosmeae representing related clades with different photosynthetic types: Threlkeldia diffusa (C3), Sedobassia sedoides (C2), and Bassia prostrata (C4). Results show that B. prostrata belongs to the NADP-ME type and core genes encoding for C4 cycle are significantly upregulated when compared with Sed. sedoides and T. diffusa. Sedobassia sedoides and B. prostrata share a number of upregulated C4-related genes; however, two C4 transporters (DIT and TPT) are found significantly upregulated only in Sed. sedoides. Combined analysis of transcription factors (TFs) of the closely related lineages (Camphorosmeae and Salsoleae) revealed that no C3-specific TFs are higher in C2 species compared with C4 species; instead, the C2 species show their own set of upregulated TFs. Taken together, our study indicates that the hypothesis of the C2 photosynthesis as a proxy towards C4 photosynthesis is questionable in Sed. sedoides and more in favour of an independent evolutionary stable state.

Keywords: Amaranthaceae; C4 photosynthesis; Caryophyllales; Chenopodiaceae; Salsola; complex trait evolution; gene regulation; transcription factor.

MeSH terms

  • Amaranthaceae / genetics*
  • Amaranthaceae / growth & development
  • Carbon / metabolism
  • Carbon Dioxide / metabolism
  • Carbon Isotopes / metabolism
  • Chenopodiaceae / genetics*
  • Chenopodiaceae / growth & development
  • Photosynthesis / genetics*
  • Phylogeny
  • Plant Leaves / genetics
  • Plant Leaves / growth & development
  • Plant Proteins / classification
  • Plant Proteins / genetics*
  • RNA-Seq
  • Transcriptome / genetics

Substances

  • Carbon Isotopes
  • Plant Proteins
  • Carbon Dioxide
  • Carbon