Skip to main content
SpringerLink
Log in

The effect of initial stomatal opening on the dynamics of biochemical and overall photosynthetic induction

  • Original Article
  • Published:
Trees Aims and scope Submit manuscript

Abstract

Key message

Initial stomatal conductance at onset of illumination and lag times before stomata start to open in response to light are decisive for the whole course of photosynthetic induction. Neglecting these effects can reverse results when comparing induction parameters within and between species.

Abstract

We analyzed stomatal behaviors, the role of initial stomatal conductance (at onset of light, g ini), and contemporaneous effects on two types of photosynthetic induction, namely “overall” (stomatal and mesophyll effects included) and “biochemical induction” (mainly RuBisCO activity). Studies were performed in sun leaves of four species (Alnus glutinosa (L.) Gaertn., Betula pubescens Ehrh., Fagus sylvatica L., and Helianthus annuus L.) differing in shade-tolerance: A species-specific g ini-threshold, namely g ini(crit), was found, being decisive for time courses of induction. When g ini was above g ini(crit), induction half-times (t 50%) were reached within 5 min, almost completely independent of stomatal limitations, and both induction types did not differ between species. Large variations in t 50% (4–36 min) were observed when g ini < g ini(crit). These correlated linearly with lag times before onset of stomatal opening in response to light (t lag). t lag is generally the longer the lower g ini. Total overall and total biochemical induction correlated highly significantly with velocities of stomatal opening. Different induction times between species occurred as a result of stomatal behavior rather than photosynthetic parameters. Any induction process is initially more limited by the biochemical component. When g ini < g ini(crit), this biochemical limitation shifts towards stomata-dominated limitation at a lower induction state. Consequentially, stomata limit the induction process over most of the induction course. When g ini > g ini(crit) and stomata open fast, then induction is (almost) completely dominated by biochemical limitations and proceeds much faster. This study confirms the very important role of g ini(crit) in photosynthetic induction irrespective of species and discusses implications for modeling.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

Γ*:

Light-independent CO2 compensation point

ΔA120 :

Increase of photosynthesis after 120 s of illumination (A–R D)

Δw:

Leaf/air vapor concentration difference

A :

Net photosynthesis

A ind :

Overall photosynthetic induction

A max :

Maximum A at full photosynthetic induction

B ind :

Biochemical photosynthetic induction

C a :

Ambient CO2 concentration

C i :

Intercellular CO2 concentration

g :

Stomatal conductance to H2O

g c :

Cuticular conductance to H2O

g ini :

g before illumination

g l :

Leaf conductance to H2O

g m :

Mesophyll conductance to CO2

g max :

g at full induction

IS120 :

Induction state after 120 s of illumination

ISA=B :

Induction state at which A ind equals B ind

m 100 :

Initial slope of the A/C i relationship at full induction

PPFD:

Photosynthetic photon flux density

R D :

Leaf respiration in darkness

R I :

Leaf respiration in light

RuBisCO:

Ribulose-1,5-bisphosphate carboxylase/oxygenase

RuBP:

Ribulose-1,5-bisphosphate

t :

Time

t 50%A and t 90%A :

Time to reach 50% and 90% of A ind

t 50%B and t 90%B :

Time to reach 50% and 90% of B ind

t 90%g :

Time to reach 90% of g max

t A=B :

Time to reach ISA=B

t lag :

Lag time in stomatal response after beginning of illumination

References

  • Allen MT, Pearcy RW (2000) Stomatal behavior and photosynthetic performance under dynamic light regimes in a seasonally dry tropical rain forest. Oecologia 122:470–478. doi:10.1007/s004420050968

    Article  CAS  PubMed  Google Scholar 

  • Assmann SM (1999) The cellular basis of guard cell sensing of rising CO2. Plant Cell Environ 22:629–637. doi:10.1046/j.1365-3040.1999.00408.x

    Article  CAS  Google Scholar 

  • Auchincloss L, Easlon HM, Levine D et al (2014) Pre-dawn stomatal opening does not substantially enhance early-morning photosynthesis in Helianthus annuus. Plant Cell Environ 37:1364–1370. doi:10.1111/pce.12241

    Article  CAS  PubMed  Google Scholar 

  • Azoulay-Shemer T, Palomares A, Bagheri A et al (2015) Guard cell photosynthesis is critical for stomatal turgor production, yet does not directly mediate CO2- and ABA-induced stomatal closing. Plant J 83:567–581. doi:10.1111/tpj.12916

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ball JT, Woodrow IE, Berry JA (1987) A model predicting stomatal conductance and its contribution to the control of photosynthesis under different environmental conditions. In: Biggins J (ed.) Progress in Photosynthesis Research. Martinus Nijhoff Publishers, Dordrecht, pp 221–224

    Chapter  Google Scholar 

  • Bazzaz FA (1979) The physiological ecology of plant succession. Ann Rev Ecol Syst 10:351–371

    Article  Google Scholar 

  • Bernacchi CJ, Singsaas EL, Pimentel C et al (2001) Improved temperature response functions for models of Rubisco-limited photosynthesis. Plant Cell Environ 24:253–259. doi:10.1046/j.1365-3040.2001.00668.x

    Article  CAS  Google Scholar 

  • Beyschlag W, Pfanz H, Ryel R (1992) Stomatal patchiness in Mediterranean evergreen sclerophylls. Phenomenology and consequences for the interpretation of the midday depression in photosynthesis and transpiration. Planta 187:546–553

    Article  CAS  PubMed  Google Scholar 

  • Bradshaw RHW, Wolf A, Møller PF (2005) Long-term succession in a Danish temperate deciduous forest. Ecography (Cop) 28:157–164. doi:10.1111/j.0906-7590.2005.03980.x

    Article  Google Scholar 

  • Brooks A, Farquhar GD (1985) Effect of temperature on the CO2/O2 specificity of ribulose-1,5-bisphosphate carboxylase/oxygenase and the rate of respiration in the light. Estimates from gas-exchange measurements on spinach. Planta 165:397–406

    Article  CAS  PubMed  Google Scholar 

  • Chazdon RL, Pearcy RW (1986) Photosynthetic responses to light variation in rainforest species. I. Induction under constant and fluctuating light conditions. Oecologia 69:517–523

    Article  PubMed  Google Scholar 

  • Damour G, Simonneau T, Cochard H, Urban L (2010) An overview of models of stomatal conductance at the leaf level. Plant Cell Environ 33:1419–1438. doi:10.1111/j.1365-3040.2010.02181.x

    PubMed  Google Scholar 

  • Douthe C, Dreyer E, Brendel O, Warren CR (2012) Is mesophyll conductance to CO2 in leaves of three Eucalyptus species sensitive to short-term changes of irradiance under ambient as well as low O2? Funct Plant Biol 39:435–448. doi:10.1071/FP11190

    Article  CAS  Google Scholar 

  • Ethier GJ, Livingston NJ (2004) On the need to incorporate sensitivity to CO2 transfer conductance into the Farquhar-von Caemmerer-Berry leaf photosynthesis model. Plant Cell Environ 27:137–153. doi:10.1111/j.1365-3040.2004.01140.x

    Article  CAS  Google Scholar 

  • Farquhar GD, Sharkey TD (1982) Stomatal Conductance and Photosynthesis. Annu Rev. Plant Physiol 33:317–345. doi:10.1146/annurev.pp.33.060182.001533

    Article  CAS  Google Scholar 

  • Farquhar GD, Wong SC (1984) An Empirical Model of Stomatal Conductance. Funct Plant Biol 11:191–210. doi:10.1071/PP9840191

    CAS  Google Scholar 

  • Flexas J, Barbour MM, Brendel O et al (2012) Mesophyll diffusion conductance to CO2: an unappreciated central player in photosynthesis. Plant Sci 193–194:70–84. doi:10.1016/j.plantsci.2012.05.009

    Article  PubMed  Google Scholar 

  • Fujita T, Noguchi K, Terashima I (2013) Apoplastic mesophyll signals induce rapid stomatal responses to CO2 in Commelina communis. New Phytol 199:395–406. doi:10.1111/nph.12261

    Article  CAS  PubMed  Google Scholar 

  • Hoad SP, Grace J, Jeffree CE (1997) Humidity response of cuticular conductance of beech (Fagus sylvatica L.) leaf discs maintained at high relative water content. J Exp Bot 48:1969–1975. doi:10.1093/jxb/48.11.1969

    Article  CAS  Google Scholar 

  • Holišová P, Zitová M, Klem K, Urban O (2012) Effect of elevated carbon dioxide concentration on carbon assimilation under fluctuating light. J Environ Qual 41:1931–1938. doi:10.2134/jeq2012.0113

    Article  PubMed  Google Scholar 

  • Jarvis PG (1976) The interpretation of the variations in leaf water potential and stomatal conductance found in canopies in the field. Philos Trans R Soc London B 273:593–610.

    Article  CAS  Google Scholar 

  • 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. doi:10.1093/jexbot/52.359.1303

    CAS  PubMed  Google Scholar 

  • Kirschbaum MUF, Pearcy RW (1988a) Gas exchange analysis of the fast phase of photosynthetic induction in Alocasia macrorrhiza. Plant Physiol 87:818–821. doi:10.1104/pp.87.4.818

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kirschbaum MUF, Pearcy RW (1988b) Gas exchange analysis of the relative importance of stomatal and biochemical factors in photosynthetic induction in Alocasia macrorrhiza. Plant Physiol 86:782–785. doi:10.1104/pp.87.4.818

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kirschbaum MUF, Gross LJ, Pearcy RW (1988) Observed and modelled stomatal responses to dynamic light environments in the shade plant Alocasia macrorrhiza. Plant Cell Environ 11:111–121

    Google Scholar 

  • Kirschbaum MUF, Küppers M, Schneider H et al (1998) Modelling photosynthesis in fluctuating light with inclusion of stomatal conductance, biochemical activation and pools of key photosynthetic intermediates. Planta 204:16–26. doi:10.1007/s004250050225

    Article  CAS  Google Scholar 

  • Kirschbaum MUF, Oja V, Laisk A (2005) The quantum yield of CO2 fixation is reduced for several minutes after prior exposure to darkness. Exploration of the underlying causes. Plant Biol 7:58–66. doi:10.1055/s-2004-830476

    Article  CAS  PubMed  Google Scholar 

  • Kobza J, Edwards GE (1987) The photosynthetic induction response in wheat leaves: net CO2 uptake, enzyme activation, and leaf metabolites. Planta 171:549–559. doi:10.1007/BF00392305

    Article  CAS  PubMed  Google Scholar 

  • Koike T (1988) Leaf structure and photosynthetic performance as related to the forest succession of deciduous broad-leaved trees. Plant Species Biol 3:77–87

    Article  Google Scholar 

  • Košvancová M, Urban O, Šprtová M et al (2009) Photosynthetic induction in broadleaved Fagus sylvatica and coniferous Picea abies cultivated under ambient and elevated CO2 concentrations. Plant Sci 177:123–130. doi:10.1016/j.plantsci.2009.04.005

    Article  Google Scholar 

  • Küppers M (1984) Carbon relations and competition between woody species in a Central European Hedgerow. I. Photosynthetic characteristics. Oecologia (Berl) 64:332–343.

    Article  Google Scholar 

  • Küppers M, Schneider H (1993) Leaf gas exchange of beech (Fagus sylvatica L.) seedlings in lightflecks: effects of fleck length and leaf temperature in leaves grown in deep and partial shade. Trees 7:160–168. doi:10.1007/BF00199617

    Article  Google Scholar 

  • Küppers M, Schulze ED (1985) An empirical model of net photosynthesis and leaf conductance for the simulation of diurnal courses of CO2 and H2O exchange. Aust J Plant Physiol 12:513–526

    Article  Google Scholar 

  • Küppers M, Wheeler AM, Küppers BIL, et al (1986) Carbon fixation in eucalypts in the field. Analysis of diurnal variations in photosynthetic capacity. Oecologia (Berl) 70:273–282.

    Article  Google Scholar 

  • Küppers M, Swan AG, Tompkins D et al (1987) A field portable system for the measurement of gas exchange of leaves under natural and controlled conditions: examples with field-grown Eucalyptus pauciflora Sieb. ex Spreng. ssp. pauciflora, E. behriana F. Muell. and Pinus radiata R. Don. Plant Cell Environ 10:425–435. doi:10.1111/1365-3040.ep11603690

    Article  Google Scholar 

  • Küppers BIL, Küppers M, Schulze ED (1988) Soil drying and its effect on leaf conductance and CO2 assimilation of Vigna unguiculata (L.) Walp. I. The response to climatic factors and to the rate of soil drying in young plants. Oecologia 75:99–104

    Article  PubMed  Google Scholar 

  • Küppers M, Timm HC, Orth F et al (1996) Effects of light environment and successional status on lightfleck use by understory trees of temperate and tropical forests. Tree Physiol 16:69–80

    Article  PubMed  Google Scholar 

  • Küppers M, Heiland I, Schneider H, Neugebauer PJ (1999) Light-flecks cause non-uniform stomatal opening—studies with special emphasis on Fagus sylvatica L. Trees 14:130. doi:10.1007/s004680050218

    Google Scholar 

  • Lawson T, Simkin AJ, Kelly G, Granot D (2014) Mesophyll photosynthesis and guard cell metabolism impacts on stomatal behaviour. New Phytol 203:1064–1081. doi:10.1111/nph.12945

    Article  CAS  PubMed  Google Scholar 

  • Lehman RH, Rice EL (1972) Effect of deficiencies of nitrogen, potassium and sulfur on chlorogenic acids and scopolin in sunflower. Amer Midl Nat 87:71–80.

    Article  CAS  Google Scholar 

  • Mansfield TA, Atkinson CJ (1990) Stomatal Behaviour in Water Stressed Plants. In: Alscher RG, Cumming JR (eds.) Stress responses in plants: adaptation and acclimation mechanisms. Wiley-Liss, New York, pp 241–264

    Google Scholar 

  • Mott KA, Peak D (2007) Stomatal patchiness and task-performing networks. Ann Bot 99:219–226. doi:10.1093/aob/mcl234

    Article  PubMed  Google Scholar 

  • Mott KA, Woodrow IE (1993) Effects of O2 and CO2 on Nonsteady-State Photosynthesis. Plant Physiol 102:859–866

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mott KA, Sibbernsen ED, Shope JC (2008) The role of the mesophyll in stomatal responses to light and CO2. Plant Cell Environ 31:1299–1306. doi:10.1111/j.1365-3040.2008.01845.x

    Article  CAS  PubMed  Google Scholar 

  • Mott KA, Berg DG, Hunt SM, Peak D (2014) Is the signal from the mesophyll to the guard cells a vapour-phase ion? Plant Cell Environ 37:1184–1191. doi:10.1111/pce.12226

    Article  CAS  PubMed  Google Scholar 

  • Naumburg E, Ellsworth DS (2000) Photosynthetic sunfleck utilization potential of understory saplings growing under elevated CO2 in FACE. Oecologia 122:163–174. doi:10.1007/PL00008844

    Article  CAS  PubMed  Google Scholar 

  • Naumburg E, Ellsworth DS (2002) Short-term light and leaf photosynthetic dynamics affect estimates of daily understory photosynthesis in four tree species. Tree Physiol 22:393–401

    Article  PubMed  Google Scholar 

  • Ögren E, Sundin U (1996) Photosynthetic responses to variable light†¯: a comparison of species from contrasting habitats. Oecologia 106:18–27

    Article  PubMed  Google Scholar 

  • Pearcy RW, Chazdon RL, Gross LI, Mott KA (1994) Photosynthetic utilization of sunflecks: a temporally patchy resource on a time scale of seconds to minutes. In: Caldwell MM, Pearcy RW (eds.) Exploitation of environmental heterogeneity by plants. Academic Press, San Diego, pp 175–208

    Chapter  Google Scholar 

  • Pearcy RW, Gross LJ, He D (1997) An improved dynamic model of photosynthesis for estimation of carbon gain in sunfleck light regimes. Plant Cell Environ 20:411–424

    Article  Google Scholar 

  • Portis AR (2003) Rubisco activase—Rubisco’s catalytic chaperone. Photosynth Res 75:11–27

    Article  CAS  PubMed  Google Scholar 

  • Pospíšilová J, Šantrůček J (1994) Stomatal patchiness. Biol Plant 36:481–510. doi:10.1007/BF02921169

    Article  Google Scholar 

  • Radin JW, Lu Z, Percy RG, Zeiger E (1994) Genetic variability for stomatal conductance in Pima cotton and its relation to improvements of heat adaptation. Proc Natl Acad Sci USA 91:7217–7221. doi:10.1073/pnas.91.15.7217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raschke K (1979) Movements of stomata. In: Haupt W, Feinleib ME (eds.) Encyclopedia of plant physiology NS, vol VII. Springer, Berlin, pp 383–441

    Google Scholar 

  • Resco de Dios V, Gessler A, Ferrio JP et al (2016) Circadian rhythms have significant effects on leaf-to-canopy scale gas exchange under field conditions. Gigascience 5:43. doi:10.1186/s13742-016-0149-y

    Article  PubMed  PubMed Central  Google Scholar 

  • Sassenrath-Cole GF, Pearcy RW (1992) The role of Ribulose-1,5-bisphosphate regeneration in the induction requirement of photosynthetic co(2) exchange under transient light conditions. Plant Physiol 99:227–234. doi:10.1104/pp.99.1.227

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seemann JR, Kirschbaum MUF, Sharkey TD, Pearcy RW (1988) Regulation of Ribulose-1,5-bisphosphate carboxylase activity in Alocasia macrorrhiza in response to step changes in irradiance. Plant Physiol 88:148–152. doi:10.1104/pp.88.1.148

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stegemann J, Timm HC, Küppers M (1999) Simulation of photosynthetic plasticity in response to highly fluctuating light: an empirical model integrating dynamic photosynthetic induction and capacity. Trees 14:145–160. doi:10.1007/s004680050219

    Article  Google Scholar 

  • Terashima I, Wong SC, Osmond CB, Farquhar GD (1988) Characterisation of non-uniform photosynthesis induced by abscisic acid in leaves having different mesophyll anatomies. Plant Cell Physiol 29:385–394

    CAS  Google Scholar 

  • Timm HC, Küppers M, Stegemann J (2004) Non-destructive analysis of architectural expansion and assimilate allocation in different tropical tree saplings: consequences of using steady-state and dynamic photosynthesis models. Ecotropica 10:101–121

    Google Scholar 

  • Tinoco-Ojanguren C, Pearcy RW (1993) Stomatal dynamics and its importance to carbon gain in two rainforest Piper species—I. VPD effects on the transient stomatal response to lightflecks. Oecologia 94:388–394. doi:10.1007/BF00317114

    Article  PubMed  Google Scholar 

  • Tomimatsu H, Tang Y (2012) Elevated CO2 differentially affects photosynthetic induction response in two Populus species with different stomatal behavior. Oecologia 169:869–878. doi:10.1007/s00442-012-2256-5

    Article  PubMed  Google Scholar 

  • Urban O, Košvancová M, Marek MV, Lichtenthaler HK (2007) Induction of photosynthesis and importance of limitations during the induction phase in sun and shade leaves of five ecologically contrasting tree species from the temperate zone. Tree Physiol 27:1207–1215. doi:10.1093/treephys/27.8.1207

    Article  PubMed  Google Scholar 

  • Urban O, Sprtová M, Košvancová M et al (2008) Comparison of photosynthetic induction and transient limitations during the induction phase in young and mature leaves from three poplar clones. Tree Physiol 28:1189–1197

    Article  CAS  PubMed  Google Scholar 

  • Valladares F, Allen MT, Pearcy RW (1997) Photosynthetic responses to dynamic light under field conditions in six tropical rainforest shrubs occuring along a light gradient. Oecologia 111:505–514. doi:10.1007/s004420050264

    Article  CAS  PubMed  Google Scholar 

  • Vialet-Chabrand S, Dreyer E, Brendel O (2013) Performance of a new dynamic model for predicting diurnal time courses of stomatal conductance at the leaf level. Plant Cell Environ 36:1529–1546. doi:10.1111/pce.12086

    Article  PubMed  Google Scholar 

  • Vico G, Manzoni S, Palmroth S, Katul G (2011) Effects of stomatal delays on the economics of leaf gas exchange under intermittent light regimes. New Phytol 192:640–652. doi:10.1111/j.1469-8137.2011.03847.x

    Article  CAS  PubMed  Google Scholar 

  • von Caemmerer S, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153:376–387. doi:10.1007/BF00384257

    Article  Google Scholar 

  • Way DA, Pearcy RW (2012) Sunflecks in trees and forests: From photosynthetic physiology to global change biology. Tree Physiol 32:1066–1081. doi:10.1093/treephys/tps064

    Article  PubMed  Google Scholar 

  • Woodrow IE, Mott KA (1989) Rate limitation of non-steady-state photosynthesis by Ribulose-1,5-bisphosphate carboxylase in Spinach. Aust J Plant Physiol 16:487. doi:10.1071/PP9890487

    Article  CAS  Google Scholar 

  • Zhang J, Davies WJ (1990) Changes in the concentration of ABA in xylem sap as a function of changing soil water status can account for changes in leaf conductance and growth. Plant Cell Environ 13:277–285

    Article  CAS  Google Scholar 

  • Zhang Q, Chen JW, Li BG, Cao KF (2009) Epiphytes and hemiepiphytes have slower photosynthetic response to lightflecks than terrestrial plants: evidence from ferns and figs. J Trop Ecol 25:465. doi:10.1017/S026646740900618X

    Article  Google Scholar 

  • Zhang Q, Chen YJ, Song LY et al (2012) Utilization of lightflecks by seedlings of five dominant tree species of different subtropical forest successional stages under low-light growth conditions. Tree Physiol 32:545–553. doi:10.1093/treephys/tps043

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Miko Kirschbaum (Palmerston North, New Zealand) and unknown reviewers for very helpful comments on an earlier version of the manuscript.

Author information

Authors and Affiliations

  1. Institute of Botany, University of Hohenheim, Garbenstrasse 30, 70599, Stuttgart, Germany

    Magnus Wachendorf & Manfred Küppers

Authors
  1. Magnus Wachendorf
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Manfred Küppers
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Magnus Wachendorf.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by A. Gessler.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wachendorf, M., Küppers, M. The effect of initial stomatal opening on the dynamics of biochemical and overall photosynthetic induction. Trees 31, 981–995 (2017). https://doi.org/10.1007/s00468-017-1522-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00468-017-1522-x

Keywords

Search

Navigation