Light and CO2/cAMP Signal Cross Talk on the Promoter Elements of Chloroplastic β-Carbonic Anhydrase Genes in the Marine Diatom Phaeodactylum tricornutum

Plant Physiol. 2016 Feb;170(2):1105-16. doi: 10.1104/pp.15.01738. Epub 2015 Dec 11.

Abstract

Our previous study showed that three CO2/cAMP-responsive elements (CCRE) CCRE1, CCRE2, and CCRE3 in the promoter of the chloroplastic β-carbonic anhydrase 1 gene in the marine diatom Phaeodactylum tricornutum (Pptca1) were critical for the cAMP-mediated transcriptional response to ambient CO2 concentration. Pptca1 was activated under CO2 limitation, but the absence of light partially disabled this low-CO2-triggered transcriptional activation. This suppression effect disappeared when CCRE2 or two of three CCREs were replaced with a NotI restriction site, strongly suggesting that light signal cross-talks with CO2 on the cAMP-signal transduction pathway that targets CCREs. The paralogous chloroplastic carbonic anhydrase gene, ptca2 was also CO2/cAMP-responsive. The upstream truncation assay of the ptca2 promoter (Pptca2) revealed a short sequence of -367 to -333 relative to the transcription-start site to be a critical regulatory region for the CO2 and light responses. This core-regulatory region comprises one CCRE1 and two CCRE2 sequences. Further detailed analysis of Pptca2 clearly indicates that two CCRE2s are the cis-element governing the CO2/light response of Pptca2. The transcriptional activation of two Pptcas in CO2 limitation was evident under illumination with a photosynthetically active light wavelength, and an artificial electron acceptor from the reduction side of PSI efficiently inhibited Pptcas activation, while neither inhibition of the linear electron transport from PSII to PSI nor inhibition of ATP synthesis showed an effect on the promoter activity, strongly suggesting a specific involvement of the redox level of the stromal side of the PSI in the CO2/light cross talk.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphate / biosynthesis
  • Aquatic Organisms / drug effects
  • Aquatic Organisms / enzymology*
  • Aquatic Organisms / genetics
  • Aquatic Organisms / radiation effects
  • Base Sequence
  • Biological Assay
  • Carbon Dioxide / pharmacology*
  • Carbonic Anhydrases / genetics*
  • Carbonic Anhydrases / metabolism
  • Diatoms / drug effects
  • Diatoms / enzymology*
  • Diatoms / genetics*
  • Diatoms / radiation effects
  • Gene Expression Regulation, Plant / drug effects
  • Gene Expression Regulation, Plant / radiation effects
  • Glucuronidase / metabolism
  • Light*
  • Photosystem I Protein Complex / metabolism
  • Photosystem II Protein Complex / metabolism
  • Promoter Regions, Genetic*
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism

Substances

  • Photosystem I Protein Complex
  • Photosystem II Protein Complex
  • RNA, Messenger
  • Carbon Dioxide
  • Adenosine Triphosphate
  • Glucuronidase
  • Carbonic Anhydrases