Nighttime transpirational cooling enabled by circadian regulation of stomatal conductance is related to stomatal anatomy and leaf morphology in rice.
Leaf morphology
Nocturnal leaf temperature
Nocturnal stomatal conductance
Oryza genus
Photosynthesis
Stomatal density
Stomatal size
Journal
Planta
ISSN: 1432-2048
Titre abrégé: Planta
Pays: Germany
ID NLM: 1250576
Informations de publication
Date de publication:
24 Jun 2021
24 Jun 2021
Historique:
received:
21
03
2021
accepted:
11
06
2021
entrez:
24
6
2021
pubmed:
25
6
2021
medline:
29
6
2021
Statut:
epublish
Résumé
Rice genotypes with larger stomata maintain higher nocturnal stomatal conductance, thus having lower nocturnal leaf temperature via transpirational cooling. Incomplete night stomatal closure has been widely observed, but the mechanisms and functions of nocturnal stomatal conductance (g
Identifiants
pubmed: 34165635
doi: 10.1007/s00425-021-03661-w
pii: 10.1007/s00425-021-03661-w
doi:
Substances chimiques
Water
059QF0KO0R
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
12Subventions
Organisme : National Key Research and Development Program of China
ID : 2016YFD0300102
Organisme : National Natural Science Foundation of China
ID : 31871532
Références
Alward RD, Detling JK, Milchunas DG (1999) Grassland vegetation changes and nocturnal global warming. Science 283:229–231
pubmed: 9880257
Auchincloss L, Easlon HM, Levine D, Donovan L, Richards JH (2014) Pre-dawn stomatal opening does not substantially enhance early-morning photosynthesis in Helianthus annuus. Plant Cell Environ 37:1364–1370
pubmed: 24895756
Barbour MM, Cernusak LA, Whitehead D, Griffin K, Turnbull M, Tissue DT, Farquhar GD (2005) Nocturnal stomatal conductance and implications for modelling δ
Bonan GB (2008) Forests and climate change: forcings, feedbacks, and the climate benefits of forests. Science 320:1444–1449
pubmed: 18556546
Bucci SJ, Scholz FB, Goldstein G, Meinzer FC, Hinojsa JA, Hoffmann WA, Franco AC (2004) Processes preventing nocturnal equilibration between leaf and soil water potential in tropical savanna woody species. Tree Physiol 24:1119–1127
pubmed: 15294758
Buckley TN, John GP, Scoffoni C, Sack L (2017) The sites of evaporation within leaves. Plant Physiol 173:1763–1782
pubmed: 28153921
pmcid: 5338672
Caine RS, Yin X, Sloan J, Harrison EL, Mohammed U, Fulton T, Biswal AK, Dionora J, Chater CC, Gray JE et al (2018) Rice with reduced stomatal density conserves water and has improved drought tolerance under future climate conditions. New Phytol 221:371–384
pubmed: 30043395
pmcid: 6492113
Caird MA, Richards JH, Donovan LA (2007) Nighttime stomatal conductance and transpiration in C3 and C4 plants. Plant Physiol 143:4–10
pubmed: 17210908
pmcid: 1761996
Caldeira CF, Jeanguenin L, Chaumont F, Tardieu F (2014) Circadian rhythms of hydraulic conductance and growth are enhanced by drought and improve plant performance. Nat Commun 5:5365
pubmed: 25370944
Chieppa J, Brown T, Giresi P, Juenger TE, Resco de Dios V, Tissue DT, Aspinwall MJ (2021) Climate and stomatal traits drive covariation in nighttime stomatal conductance and daytime gas exchange rates in a widespread C4 grass. New Phytol 229:2020–2034
pubmed: 33037633
Christman MA, Richards JH, McKay JK, Stahl EA, Juenger TE, Donovan LA (2008) Genetic variation in Arabidopsis thaliana for night-time leaf conductance. Plant Cell Environ 31:1170–1178
pubmed: 18510710
Claverie E, Meunier F, Javaux M, Sadok W (2018) Increased contribution of wheat nocturnal transpiration to daily water use under drought. Physiol Plant 162:290–300
pubmed: 28833246
Costa JM, Monnet F, Jannaud D, Leonhardt N, Ksas B, Reiter IM, Pantin F, Genty B (2015) Open all night long: the dark side of stomatal control. Plant Physiol 167:289–294
pubmed: 25527716
Coupel-Ledru A, Lebon E, Christophe A, Gallo A, Gago P, Pantin F, Doligez A, Simonneau T (2016) Reduced nighttime transpiration is a relevant breeding target for high water-use efficiency in grapevine. Proc Natl Acad Sci USA 113:8963–8968
pubmed: 27457942
pmcid: 4987834
Cowan IR, Farquhar GD (1977) Stomatal function in relation to leaf metabolism and environment. In: Jennings DH (ed) Integration of activity in the higher plant. Cambridge University Press, Cambridge, pp 471–505
Daley MJ, Phillips NG (2006) Interspecific variation in nighttime transpiration and stomatal conductance in a mixed New England deciduous forest. Tree Physiol 26:411–419
pubmed: 16414920
Doheny-Adams T, Hunt L, Franks PJ, Beerling DJ, Gray JE (2012) Genetic manipulation of stomatal density influences stomatal size, plant growth and tolerance to restricted water supply across a growth carbon dioxide gradient. Phil Trans R Soc B 367:547–555
pubmed: 22232766
pmcid: 3248714
Donovan LA, Linton MJ, Richards JH (2001) Predawn plant water potential does not necessarily equilibrate with soil water potential under well-watered conditions. Oecologia 129:328–335
pubmed: 28547187
Drake JE, Tjoelker MG, Varhammar A, Medlyn BE, Reich PB, Leigh A, Pfautsch S, Blackman CJ, Lopez R, Barton CVM et al (2018) Trees tolerate an extreme heatwave via sustained transpirational cooling and increased leaf thermal tolerance. Glob Change Biol 24:2390–2402
Dunbar-Co S, Sporck MJ, Sack L (2009) Leaf trait diversification and design in seven rare taxa of the Hawaiian Plantago radiation. Int J Plant Sci 170:61–75
Ehrler WL (1971) Periodic nocturnal stomatal opening of citrus in a steady environment. Physiol Plant 25:488–492
Even M, Sabo M, Meng D, Kreszies T, Schreiber L, Fricke W (2018) Nighttime transpiration in barley (Hordeum vulgare) facilitates respiratory carbon dioxide release and is regulated during salt stress. Ann Bot 122:569–582
pubmed: 29850772
pmcid: 6153476
Franks PJ, Beerling DJ (2009) Maximum leaf conductance driven by CO
pubmed: 19506250
pmcid: 2693183
Fricke W (2019) Night-time transpiration – favouring growth? Trends Plant Sci 24:311–317
pubmed: 30770287
Furbank RT, Tester M (2011) Phenomics—technologies to relieve the phenotyping bottleneck. Trends Plant Sci 16:635–644
pubmed: 22074787
Gates DW (1968) Transpiration and leaf temperature. Annu Rev Plant Physiol 191:211–238
Grace J, Fasehun FE, Dixon M (1980) Boundary layer conductance of the leaves of some tropical timber trees. Plant Cell Environ 3:443–450
Grant OM, Tronina L, Jones HG, Chaves MM (2007) Exploring thermal imaging variables for the detection of stress responses in grapevine under different irrigation regimes. J Exp Bot 58:815–825
pubmed: 17032729
Guilioni L, Jones HG, Leinonen I, Lhomme JP (2008) On the relationships between stomatal resistance and leaf temperatures in thermography. Agr for Meteorol 148:1908–1912
Hassidim M, Dakhiya Y, Turjeman A, Hussien D, Shor E, Anidjar A, Goldberg K, Green R (2017) CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) and the circadian control of stomatal aperture. Plant Physiol 175:1864–1877
pubmed: 29084902
pmcid: 5717738
Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424:901–908
pubmed: 12931178
Hill KE, Hill RS, Watling R (2019) Pinnule and stomatal size and stomatal density of living and fossil Bowenia and Eobowenia specimens give insight into physiology during cretaceous and eocene paleoclimates. Int J Plant Sci 180:323–336
Jerbi A, Brereton NJB, Amiot ESS, Lachapelle-T X, Comeau Y, Pitre FE, Labrecque M (2020) High biomass yield increases in a primary effluent wastewater phytofiltration are associated to altered leaf morphology and stomatal size in Salix miyabeana. Sci Total Environ 738:139728
pubmed: 32534285
Kaiser H, Kappen L (2000) In situ observation of stomatal movements and gas exchange of Aegopodium podagraria L. in the understorey. J Exp Bot 51:1741–1749
pubmed: 11053464
Kaiser H, Kappen L (2001) Stomatal oscillations at small apertures: indications for a fundamental insufficiency of stomatal feedback-control inherent in the stomatal turgor mechanism. J Exp Bot 52:1303–1313
pubmed: 11432949
Lasceve G, Leymarie J, Vavasseur A (1997) Alterations in light-induced stomatal opening in a starch-deficient mutant of Arabidopsis thaliana L. deficient in chloroplast phosphoglucomutase activity. Plant Cell Environ 20:350–358
Leigh A, Sevanto S, Ball MC, Close JD, Ellsworth DS, Knight CA, Nicotra AB, Vogel S (2012) Do thick leaves avoid thermal damage in critically low wind speeds? New Phytol 194:477–487
pubmed: 22296328
Leigh A, Sevanto S, Close JD, Nicotra AB (2017) The influence of leaf size and shape on leaf thermal dynamics: does theory hold up under natural conditions? Plant Cell Environ 40:237–248
pubmed: 28026874
Levine L, Richards J, Wheeler R (2009) Super-elevated CO
pubmed: 19131142
Lobell D, Schlenke W, Costa-Roberts J (2011) Climate trends and global crop production since 1980. Science 333:616–620
pubmed: 21551030
Marks CO, Lechowicz M (2007) The ecological and functional correlates of nocturnal transpiration. Tree Physiol 27:577–584
pubmed: 17241999
Martin TA, Hinckley TM, Meinzer FC, Sprugel DG (1999) Boundary layer conductance, leaf temperature and transpiration of Abies amabilis branches. Tree Physiol 19:435–443
pubmed: 12651549
Medlyn BE, Duursma RA, Eamus D, Ellsworth DS, Prentice IC, Barton MC, Crous KY, Angelis PD, Freeman M, Wingate L (2011) Reconciling the optimal and empirical approaches to modelling stomatal conductance. Glob Change Biol 17:2134–2144
Merlot S, Mustilli AC, Genty B, North H, Lefebvre V, Sotta B, Vavasseur A, Giraudat J (2002) Use of infrared thermal imaging to isolate Arabidopsis mutants defective in stomatal regulation. Plant J 30:601–609
pubmed: 12047634
Ogle K, Lucas RW, Bentley LP, Cable JM, Barron-Gafford GA, Griffith A, Ignace D, Jenerette GD, Tyler A, Huxman TE et al (2012) Differential daytime and night-time stomatal behavior in plants from North American deserts. New Phytol 194:464–476
pubmed: 22348404
Ouyang W, Struik PC, Yin X, Yang J (2017) Stomatal conductance, mesophyll conductance, and transpiration effciency in relation to leaf anatomy in rice and wheat genotypes under drought. J Exp Bot 68:5191–5205
pubmed: 28992130
pmcid: 5853379
Palet A, Ribas-Carbo M, Argiles JM, Azcon-Bieto J (1991) Short-term effects of carbon dioxide on carnation callus cell respiration. Plant Physiol 96:467–472
pubmed: 16668209
pmcid: 1080793
Parkhurst DF, Loucks OL (1972) Optimal leaf size in relation to environment. J Ecol 60:505–537
Peng S, Huang J, Sheehy JE, Laza RC, Visperas RM, Zhong X, Centeno GS, Khush GS, Cassman KG (2004) Rice yields decline with higher night temperature from global warming. Proc Natl Acad Sci USA 101:9971–9975
pubmed: 15226500
pmcid: 454199
Peppe DJ, Royer DL, Cariglino B, Oliver S, Newman S, Leight E, Enikolopov G, Fernandez-Burgos M, Herrera F, Wright IJ et al (2011) Sensitivity of leaf size and shape to climate: global patterns and paleoclimatic applications. New Phytol 190:724–739
pubmed: 21294735
Resco de Dios V, Diaz-Sierra R, Goulden ML, Barton CV, Boer MM, Gessler A, Ferrio JP, Pfautsch S, Tissue DT (2013) Woody clockworks: circadian regulation of night-time water use in Eucalyptus globulus. New Phytol 200:743–752
pubmed: 23795820
Resco de Dios V, Roy J, Ferrio JP, Alday JG, Landais D, Milcu A, Gessler A (2015) Processes driving nocturnal transpiration and implications for estimating land evapotranspiration. Sci Rep 5:10975
Resco de Dios V, Loik ME, Smith RA, Aspinwall MJ, Tissue DT (2016) Genetic variation in circadian regulation of nocturnal stomatal conductance enhances plant fitness. Plant Cell Environ 39:3–11
pubmed: 26147129
Resco de Dios V, Chowdhury FI, Franda E, Yao Y, Tissue DT (2019) Assessing the potential functions of nocturnal stomatal conductance in C3 and C4 plants. New Phytol 223:1696–1706
pubmed: 31055839
Rogiers SY, Clarke SJ (2013) Nocturnal and daytime stomatal conductance respond to root-zone temperature in ‘Shiraz’ grapevines. Ann Bot 111:433–444
pubmed: 23293018
pmcid: 3579449
Rohula G, Kupper P, Räim O, Sellin A, Sõber A (2014) Patterns of nighttime water use are interrelated with leaf nitrogen concentration in shoots of 16 deciduous woody species. Environ Exp Bot 99:180–188
Sack L, Scoffoni C (2011) Minimum epidermal conductance (g
Sack L, Cowan PD, Jaikumar N, Holbrook NM (2003) The ‘hydrology’ of leaves: co-ordination of structure and function in temperate woody species. Plant Cell Environ 26:1343–1356
Sadok W, Jagadish SVK (2020) The hidden costs of nighttime warming on yields. Trends Plant Sci 25:644–651
pubmed: 32526169
Schoppach R, Claverie E, Sadok W (2014) Genotype-dependent influence of night-time vapour pressure deficit on night-time transpiration and daytime gas exchange in wheat. Funct Plant Biol 41:963–971
pubmed: 32481049
Schuler ML, Sedelnikova OV, Walker BJ, Westhoff P, Langdale JA (2018) SHORTROOT-mediated increase in stomatal density has no impact on photosynthetic efficiency. Plant Physiol 176:757–772
pubmed: 29127261
Sirault XRR, James RA, Furbank RT (2009) A new screening method for osmotic component of salinity tolerance in cereals using infrared thermography. Funct Plant Biol 36:970–977
pubmed: 32688708
Smith WK (1978) Temperatures of desert plants: Another perspective on the adaptability of leaf size. Science 201:614–616
pubmed: 17794122
Sun Y, Yan F, Cui X, Liu F (2014) Plasticity in stomatal size and density of potato leaves under different irrigation and phosphorus regimes. J Plant Physiol 171:1248–1255
pubmed: 25014260
Tamang BG, Sadok W (2018) Nightly business: links between daytime canopy conductance, nocturnal transpiration and its circadian control illuminate physiological trade-offs in maize. Environ Exp Bot 148:192–202
Wang Y, Anderegg WR, Venturas MD, Trugman AT, Yu K, Frankenberg C (2021) Optimization theory explains nighttime stomatal responses. New Phytol 230:1550–1561
pubmed: 33576001
Wright IJ, Dong N, Maire V, Prentice IC, Westoby M, Díaz S, Gallagher RV, Jacobs BF, Kooyman R, Wilf P et al (2017) Global climatic drivers of leaf size. Science 357:917–921
pubmed: 28860384
Xiong D, Flexas J, Yu T, Peng S, Huang J (2017) Leaf anatomy mediates coordination of leaf hydraulic conductance and mesophyll conductance to CO
pubmed: 27653809
Yu K, Goldsmith GR, Wang Y, Anderegg WRL (2019) Phylogenetic and biogeographic controls of plant nighttime stomatal conductance. New Phytol 222:1778–1788
pubmed: 30779147
Zhang Q, Peng S, Li Y (2019) Increase rate of light-induced stomatal conductance is related to stomatal size in the genus Oryza. J Exp Bot 70:5259–5269
pubmed: 31145797
pmcid: 6793446