C4 and crassulacean acid metabolism within a single leaf: deciphering key components behind a rare photosynthetic adaptation

New Phytol. 2020 Feb;225(4):1699-1714. doi: 10.1111/nph.16265. Epub 2019 Nov 16.

Abstract

Although biochemically related, C4 and crassulacean acid metabolism (CAM) systems are expected to be incompatible. However, Portulaca species, including P. oleracea, operate C4 and CAM within a single leaf, and the mechanisms behind this unique photosynthetic arrangement remain largely unknown. Here, we employed RNA-seq to identify candidate genes involved exclusively or shared by C4 or CAM, and provided an in-depth characterization of their transcript abundance patterns during the drought-induced photosynthetic transitions in P. oleracea. Data revealed fewer candidate CAM-specific genes than those recruited to function in C4 . The putative CAM-specific genes were predominantly involved in night-time primary carboxylation reactions and malate movement across the tonoplast. Analysis of gene transcript-abundance regulation and photosynthetic physiology indicated that C4 and CAM coexist within a single P. oleracea leaf under mild drought conditions. Developmental and environmental cues were shown to regulate CAM expression in stems, whereas the shift from C4 to C4 -CAM hybrid photosynthesis in leaves was strictly under environmental control. Moreover, efficient starch turnover was identified as part of the metabolic adjustments required for CAM operation in both organs. These findings provide insights into C4 /CAM connectivity and compatibility, contributing to a deeper understanding of alternative ways to engineer CAM into C4 crop species.

Keywords: Portulaca oleracea; C4; RNA-seq; crassulacean acid metabolism; drought stress; facultative CAM; transcriptome.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Adaptation, Physiological
  • Arabidopsis Proteins / physiology*
  • Chlorophyll A / genetics
  • Chlorophyll A / metabolism
  • Crassulacean Acid Metabolism / physiology*
  • Gene Expression Regulation, Plant / physiology
  • Photosystem II Protein Complex / physiology*
  • Plant Leaves / metabolism*
  • Plant Stems / physiology
  • Plant Transpiration
  • Portulaca / physiology*
  • RNA, Plant / genetics
  • RNA, Plant / metabolism

Substances

  • Arabidopsis Proteins
  • PSB33 protein, Arabidopsis
  • Photosystem II Protein Complex
  • RNA, Plant
  • Chlorophyll A