Respiration in leaves and the continued elevation in the atmospheric
- Award ID(s):
- 1900567
- NSF-PAR ID:
- 10321393
- Date Published:
- Journal Name:
- Proceedings of the National Academy of Sciences
- Volume:
- 118
- Issue:
- 47
- ISSN:
- 0027-8424
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
Summary CO 2concentration causeCO 2‐mediated reduction in stomatal pore apertures. Several mutants have been isolated for which stomatal responses to both abscisic acid (ABA ) andCO 2are simultaneously defective. However, there are only few mutations that impair the stomatal response to elevatedCO 2, but not toABA . Such mutants are invaluable in unraveling the molecular mechanisms of earlyCO 2signal transduction in guard cells. Recently, mutations in the mitogen‐activated protein (MAP ) kinase, , have been shown to partially impairMPK 12CO 2‐induced stomatal closure. Here, we show thatmpk12 plants, in which is stably silenced specifically in guard cells (MPK 4mpk12 mpk4 homozygous double‐mutants), completely lackGC CO 2‐induced stomatal responses and have impaired activation of guard cell S‐type anion channels in response to elevatedCO 2/bicarbonate. However,ABA ‐induced stomatal closure, S‐type anion channel activation andABA ‐induced marker gene expression remain intact in thempk12 mpk4 double‐mutants. These findings suggest thatGC MPK 12 andMPK 4 act very early inCO 2signaling, upstream of, or parallel to the convergence ofCO 2andABA signal transduction. The activities ofMPK 4 andMPK 12 protein kinases were not directly modulated byCO 2/bicarbonatein vitro , suggesting that they are not directCO 2/bicarbonate sensors. Further data indicate thatMPK 4 andMPK 12 have distinguishable roles in Arabidopsis and that the previously suggested role ofRHC 1 in stomatalCO 2signaling is minor, whereasMPK 4 andMPK 12 act as key components of early stomatalCO 2signal transduction. -
Stomatal pore apertures are narrowing globally due to the continuing rise in atmospheric [CO2]. CO2elevation and the plant hormone abscisic acid (ABA) both induce rapid stomatal closure. However, the underlying signal transduction mechanisms for CO2/ABA interaction remain unclear. Two models have been considered: (
i ) CO2elevation enhances ABA concentrations and/or early ABA signaling in guard cells to induce stomatal closure and (ii ) CO2signaling merges with ABA at OST1/SnRK2.6 protein kinase activation. Here we use genetics, ABA-reporter imaging, stomatal conductance, patch clamp, and biochemical analyses to investigate these models. The strong ABA biosynthesis mutantsnced3/nced5 andaba2-1 remain responsive to CO2elevation. Rapid CO2-triggered stomatal closure in PYR/RCAR ABA receptor quadruple and hextuple mutants is not disrupted but delayed. Time-resolved ABA concentration monitoring in guard cells using a FRET-based ABA-reporter, ABAleon2.15, and ABA reporter gene assays suggest that CO2elevation does not trigger [ABA] increases in guard cells, in contrast to control ABA exposures. Moreover, CO2activates guard cell S-type anion channels innced3/nced5 and ABA receptor hextuple mutants. Unexpectedly, in-gel protein kinase assays show that unlike ABA, elevated CO2does not activate OST1/SnRK2 kinases in guard cells. The present study points to a model in which rapid CO2signal transduction leading to stomatal closure occurs via an ABA-independent pathway downstream of OST1/SnRK2.6. Basal ABA signaling and OST1/SnRK2 activity are required to facilitate the stomatal response to elevated CO2. These findings provide insights into the interaction between CO2/ABA signal transduction in light of the continuing rise in atmospheric [CO2]. -
Summary Low concentrations of CO2cause 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 CO2response 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 thatcpk3/5/6/11/23 quintuple mutant plants, but not other analyzedcpk 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 incpk3/5/6/11/23 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‐targetedcbl1/4/5/8/9 quintuple mutant plants.Our findings describe combinatorial
cpk mutants that function in CO2control of stomatal movements and support the results of classical studies showing a role for Ca2+in this response. -
SUMMARY Jasmonic acid (JA) and salicylic acid (SA) regulate stomatal closure, preventing pathogen invasion into plants. However, to what extent abscisic acid (ABA), SA and JA interact, and what the roles of SA and JA are in stomatal responses to environmental cues, remains unclear. Here, by using intact plant gas‐exchange measurements in JA and SA single and double mutants, we show that stomatal responsiveness to CO2, light intensity, ABA, high vapor pressure deficit and ozone either did not or, for some stimuli only, very slightly depended upon JA and SA biosynthesis and signaling mutants, including
dde2, sid2, coi1 ,jai1 ,myc2 andnpr1 alleles. Although the stomata in the mutants studied clearly responded to ABA, CO2, light and ozone, ABA‐triggered stomatal closure innpr1‐1 was slightly accelerated compared with the wild type. Stomatal reopening after ozone pulses was quicker in thecoi1‐16 mutant than in the wild type. In intact Arabidopsis plants, spraying with methyl‐JA led to only a modest reduction in stomatal conductance 80 min after treatment, whereas ABA and CO2induced pronounced stomatal closure within minutes. We could not document a reduction of stomatal conductance after spraying with SA. Coronatine‐induced stomatal opening was initiated slowly after 1.5–2.0 h, and reached a maximum by 3 h after spraying intact plants. Our results suggest that ABA, CO2and light are major regulators of rapid guard cell signaling, whereas JA and SA could play only minor roles in the whole‐plant stomatal response to environmental cues in Arabidopsis andSolanum lycopersicum (tomato). -
A central question is how specificity in cellular responses to the eukaryotic second messenger Ca2+ is achieved. Plant guard cells, that form stomatal pores for gas exchange, provide a powerful system for in depth investigation of Ca2+-signaling specificity in plants. In intact guard cells, abscisic acid (ABA) enhances (primes) the Ca2+-sensitivity of downstream signaling events that result in activation of S-type anion channels during stomatal closure, providing a specificity mechanism in Ca2+-signaling. However, the underlying genetic and biochemical mechanisms remain unknown. Here we show impairment of ABA signal transduction in stomata of calcium-dependent protein kinase quadruple mutant plants. Interestingly, protein phosphatase 2Cs prevent non-specific Ca2+-signaling. Moreover, we demonstrate an unexpected interdependence of the Ca2+-dependent and Ca2+-independent ABA-signaling branches and the in planta requirement of simultaneous phosphorylation at two key phosphorylation sites in SLAC1. We identify novel mechanisms ensuring specificity and robustness within stomatal Ca2+-signaling on a cellular, genetic, and biochemical level.