A role for calcium-dependent protein kinases in differential CO2- and ABA-controlled stomatal closing and low CO2-induced stomatal opening in Arabidopsis

Sebastian Schulze, Guillaume Dubeaux, Paulo H.O. Ceciliato, Shintaro Munemasa, Maris Nuhkat, Dmitry Yarmolinsky, Jaimee Aguilar, Renee Diaz, Tamar Azoulay-Shemer, Leonie Steinhorst, Jan Niklas Offenborn, Jörg Kudla, Hannes Kollist, Julian I. Schroeder

Research output: Contribution to journalArticlepeer-review

Abstract

Low concentrations of CO2 cause stomatal opening, whereas [CO2] elevation leads to stomatal closure. Classical studies have suggested a role for Ca2+ and protein phosphorylation in CO2-induced stomatal closing. Calcium-dependent protein kinases (CPKs) and calcineurin-B-like proteins (CBLs) can sense and translate cytosolic elevation of the second messenger Ca2+ into specific phosphorylation events. However, Ca2+-binding proteins that function in the stomatal CO2 response remain unknown. Time-resolved stomatal conductance measurements using intact plants, and guard cell patch-clamp experiments were performed. We isolated cpk quintuple mutants and analyzed stomatal movements in response to CO2, light and abscisic acid (ABA). Interestingly, we found that cpk3/5/6/11/23 quintuple mutant plants, but not other analyzed cpk quadruple/quintuple mutants, were defective in high CO2-induced stomatal closure and, unexpectedly, also in low CO2-induced stomatal opening. Furthermore, K+-uptake-channel activities were reduced in cpk3/5/6/11/23 quintuple mutants, in correlation with the stomatal opening phenotype. However, light-mediated stomatal opening remained unaffected, and ABA responses showed slowing in some experiments. By contrast, CO2-regulated stomatal movement kinetics were not clearly affected in plasma membrane-targeted cbl1/4/5/8/9 quintuple mutant plants. Our findings describe combinatorial cpk mutants that function in CO2 control of stomatal movements and support the results of classical studies showing a role for Ca2+ in this response.

Original languageEnglish
Pages (from-to)2765-2779
Number of pages15
JournalNew Phytologist
Volume229
Issue number5
DOIs
Publication statusPublished - Mar 2021

Keywords

  • Arabidopsis
  • abscisic acid (ABA)
  • calcineurin B-like proteins (CBLs)
  • calcium
  • calcium-dependent protein kinases (CPKs)
  • carbon dioxide (CO)
  • gas exchange
  • guard cells

ASJC Scopus subject areas

  • Physiology
  • Plant Science

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