Skip to main content
Springer Nature Link
Log in

The arc mutants of Arabidopsis with fewer large chloroplasts have a lower mesophyll conductance

  • Regular Paper
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

Photosynthetic cells of most land plant lineages have numerous small chloroplasts even though most algae, and even the early diverging land plant group the hornworts, tend to have one or a few large chloroplasts. One constraint that small chloroplasts could improve is the resistance to CO2 diffusion from the atmosphere to the chloroplast stroma. We examined the mesophyll conductance (inverse of the diffusion resistance) of mutant Arabidopsis thaliana plants with one or only a few large chloroplasts per cell. The accumulation and replication of chloroplasts (arc) mutants of A. thaliana were studied by model fitting to gas exchange data and 13CO2 discrimination during carbon fixation. The two methods generally agreed, but the value of the CO2 compensation point of Rubisco (Γ *) used in the model had a large impact on the estimated photosynthetic parameters, including mesophyll conductance. We found that having only a few large chloroplasts per cell resulted in a 25–50 % reduction in the mesophyll conductance at ambient CO2.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

References

  • Ahmadabadi M, Bock R (2012) Plastid division and morphology in the genus Peperomia. Biol Plant 56:301–306

    Article  Google Scholar 

  • Atkin OK, Evans JR, Ball MC, Lambers H, Pons TL (2000) Leaf respiration of snow gum in the light and dark. Interactions between temperature and irradiance. Plant Physiol 122:915–924

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Austin J II, Webber AN (2005) Photosynthesis in Arabidopsis thaliana mutants with reduced chloroplast number. Photosynth Res 85:373–384

    Article  CAS  Google Scholar 

  • Barbour MM, McDowell NG, Tcherkez G, Bickford CP, Hanson DT (2007) A new measurement technique reveals rapid post-illumination changes in the carbon isotope composition of leaf-respired CO2. Plant Cell Environ 30:469–482

    Article  CAS  PubMed  Google Scholar 

  • Bernacchi CJ, Singsaas EL, Pimentel C, Portis AR Jr, Long SP (2001) Improved temperature response functions for models of Rubisco-limited photosynthesis. Plant Cell Environ 24:253–259

    Article  CAS  Google Scholar 

  • Bernacchi CJ, Portis AR, Nakano H, Von Caemmerer S, Long SP (2002) Temperature response of mesophyll conductance. Implications for the determination of Rubisco enzyme kinetics and for limitations to photosynthesis in vivo. Plant Physiol 130:1992–1998

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bickford CP, McDowell NG, Erhardt EB, Hanson DT (2009) High-frequency field measurements of diurnal carbon isotope discrimination and internal conductance in a semi-arid species, Juniperus monosperma. Plant Cell Environ 32:796–810

    Article  CAS  PubMed  Google Scholar 

  • Brooks A, Farquhar GD (1985) Effects of temperature on the O2/CO2 secificity 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 

  • Busch FA, Sage TL, Cousins AB, Sage RF (2013) C3 plants enhance rates of photosynthesis by reassimilating photorespired and respired CO2. Plant Cell Environ 36:200–212

    Article  CAS  PubMed  Google Scholar 

  • Crumpton-Taylor M, Grandison S, Png KMY, Bushby AJ, Smith AM (2012) Control of starch granule numbers in Arabidopsis chloroplasts. Plant Physiol 158:905–916

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Erhardt EB, Hanson DT (2013) tdllicor: TDL/Licor Processing. R Package Version 0.1-22

  • 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

    Article  CAS  Google Scholar 

  • Evans JR, Von Caemmerer S (2013) Temperature response of carbon isotope discrimination and mesophyll conductance in tobacco. Plant Cell Environ 36:745–756

    Article  CAS  PubMed  Google Scholar 

  • Evans JR, Sharkey TD, Berry JA, Farquhar GD (1986) Carbon isotope discrimination measured concurrently with gas exchange to investigate CO2 diffusion in leaves of higher plants. Aust J Plant Physiol 13:281–292

    Article  CAS  Google Scholar 

  • Evans JR, Von Caemmerer S, Setchell BA, Hudson GS (1994) The relationship between CO2 transfer conductance and leaf anatomy in transgenic tobacco with a reduced content of Rubisco. Aust J Plant Physiol 21:475–495

    Article  CAS  Google Scholar 

  • Farquhar GD, Von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90

    Article  CAS  PubMed  Google Scholar 

  • Flexas J et al (2006) Tobacco aquaporin NtAQP1 is involved in mesophyll conductance to CO2 in vivo. Plant J 48:427–439

    Article  CAS  PubMed  Google Scholar 

  • Flexas J, Diaz-Espejo A, Galmés J, Kaldenhoff R, Medrano H, Ribas-Carbo M (2007a) Rapid variations of mesophyll conductance in response to changes in CO2 concentration around leaves. Plant Cell Environ 30:1284–1298

    Article  CAS  PubMed  Google Scholar 

  • Flexas J, Ortuño MF, Ribas-Carbo M, Diaz-Espejo A, Flórez-Sarasa ID, Medrano H (2007b) Mesophyll conductance to CO2 in Arabidopsis thaliana. New Phytol 175:501–511

    Article  CAS  PubMed  Google Scholar 

  • Graham LE, Wilcox LW (2000) Algae. Prentice Hall, Upper Saddle River

    Google Scholar 

  • Griffiths H, Helliker BR (2013) Mesophyll conductance: internal insights of leaf carbon exchange. Plant Cell Environ 36:733–735

    Article  CAS  PubMed  Google Scholar 

  • Gu L, Sun Y (2014) Artefactual responses of mesophyll conductance to CO2 and irradiance estimated with the variable J and online isotope discrimination methods. Plant Cell Environ 37(5):1231–1249

    Article  CAS  PubMed  Google Scholar 

  • Hanson DT, Renzaglia K, Villarreal JC (2014) Diffusion limitation and CO2 concentrating mechanisms in bryophytes. In: Hanson DT, Rice SK (eds) Photosynthesis in bryophytes and early land plants. Advances in photosynthesis and respiration, vol 37. Springer, Dordrecht, pp 95–111. doi:10.1007/978-94-007-6988-5_6

  • Harley PC, Loreto F, Di Marco G, Sharkey TD (1992a) Theoretical considerations when estimating the mesophyll conductance to CO2 flux by analysis of the response of photosynthesis to CO2. Plant Physiol 98:1429–1436

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Harley PC, Thomas RB, Reynolds JF, Strain BR (1992b) Modelling photosynthesis of cotton grown in elevated CO2 Plant. Cell Environ 15:271–282

    Article  CAS  Google Scholar 

  • Heckwolf M, Pater D, Hanson DT, Kaldenhoff R (2011) The Arabidopsis thaliana aquaporin AtPIP1;2 is a physiologically relevant CO2 transport facilitator. Plant J 67:795–804

    Article  CAS  PubMed  Google Scholar 

  • Jeong WJ, Park Y-I, Suh K, Raven JA, Yoo OJ, Liu JR (2002) A large population of small chloroplasts in tobacco leaf cells allows more effective chloroplast movement than a few enlarged chloroplasts. Plant Physiol 129:112–121

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jones HG, Slatyer RO (1972) Estimation of the transport and carboxylation components of the intracellular limitation to leaf photosynthesis. Plant Physiol 50:283–288

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Laisk A (1977) Kinetics of photosynthesis and photorespiration of C3 plants (in Russian). Nauka, Moscow

    Google Scholar 

  • Lanigan GJ, Betson N, Griffiths H, Seibt U (2008) Carbon isotope fractionation during photorespiration and carboxylation in Senecio. Plant Physiol 148:2013–2020

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Li Y, Ren BB, Ding L, Shen QR, Peng SB, Guo SW (2013) Does chloroplast size influence photosynthetic nitrogen use efficiency? PLoS One 8(4):e62036

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Loreto F, Harley PC, Di Marco G, Sharkey TD (1992) Estimation of mesophyll conductance to CO2 flux by three different methods. Plant Physiol 98:1437–1443

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Morita MT, Nakamura M (2012) Dynamic behavior of plastids related to environmental response. Curr Opin Plant Biol 15:722–728

    Article  CAS  PubMed  Google Scholar 

  • Osteryoung KW, Pyke KA (2014) Division and dynamic morphology of plastids. Annu Rev Plant Biol 65:443–472

    Article  CAS  PubMed  Google Scholar 

  • Possingham JV, Saurer W (1969) Changes in chloroplast number per cell during leaf development in spinach. Planta 86:186–194

    Article  CAS  PubMed  Google Scholar 

  • Psaras GK, Diamantopoulos GS, Makrypoulias CP (1996) Chlopoplast arrangement along intercellular air spaces. Isr J Plant Sci 44:1–9

    Article  Google Scholar 

  • Pyke KA (1999) Plastid division and development. Plant Cell 11:549–556

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pyke KA, Leech RM (1992) Chloroplast division and expansion is radically altered by nuclear mutations in Arabidopsis thaliana. Plant Physiol 99:1005–1008

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pyke KA, Leech RM (1994) A genetic-analysis of chloroplast division and expansion in Arabidopsis thaliana. Plant Physiol 104:201–207

    PubMed Central  CAS  PubMed  Google Scholar 

  • Pyke KA, Rutherford SM, Robertson EJ, Leech RM (1994) arc6, a fertile Arabidopsis mutant with only 2 mesophyll cell chloroplasts. Plant Physiol 106:1169–1177

    PubMed Central  CAS  PubMed  Google Scholar 

  • Samsuddin Z, Impens I (1979) Photosynthesis and diffusion resistances to carbon dioxide in Hevea brasiliensis muel. agr. clones. Oecologia 37:361–363

    Article  Google Scholar 

  • Scafaro AP, von Caemmerer S, Evans JR, Atwell BJ (2011) Temperature response of mesophyll conductance in cultivated and wild Oryza species with contrasting mesophyll cell wall thickness. Plant Cell Environ 34:1999–2008

    Article  CAS  PubMed  Google Scholar 

  • Sharkey TD (2012) Mesophyll conductance: constraint on carbon acquisition by C3 plants. Plant Cell Environ 35:1881–1883

    Article  CAS  PubMed  Google Scholar 

  • Sharkey TD, Vassey TL, Vanderveer PJ, Vierstra RD (1991) Carbon metabolism enzymes and photosynthesis in transgenic tobacco (Nicotiana tabacum L.) having excess phytochrome. Planta 185:287–296

    Article  CAS  PubMed  Google Scholar 

  • Sharkey TD, Bernacchi CJ, Farquhar GD, Singsaas EL (2007) Fitting photosynthetic carbon dioxide response curves for C3 leaves. Plant Cell Environ 30:1035–1040

    Article  CAS  PubMed  Google Scholar 

  • Takagi S (2003) Actin-based photo-orientation movement of chloroplasts in plant cells. J Exp Biol 206:1963–1969

    Article  CAS  PubMed  Google Scholar 

  • Terashima I, Miyazawa S-I, Hanba YT (2001) Why are sun leaves thicker than shade leaves? —Consideration based on analyses of CO2 diffusion in the leaf. J Plant Res 114:93–105

    Article  CAS  Google Scholar 

  • Tholen D, Boom C, Noguchi KO, Ueda S, Katase T, Terashima I (2008) The chloroplast avoidance response decreases internal conductance to CO2 diffusion in Arabidopsis thaliana leaves. Plant Cell Environ 31:1688–1700

    Article  CAS  PubMed  Google Scholar 

  • Tholen D, Boom C, Zhu X-G (2012) Opinion: prospects for improving photosynthesis by altering leaf anatomy. Plant Sci 197:92–101

    Article  CAS  PubMed  Google Scholar 

  • Uehlein N, Otto B, Hanson DT, Fischer M, McDowell N, Kaldenhoff R (2008) Function of Nicotiana tabacum aquaporins as chloroplast gas pores challenges the concept of membrane CO2 permeability. Plant Cell 20:648–657

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Villar R, Held AA, Merino J (1995) Dark leaf respiration in light and darkness of an evergreen and a deciduous plant species. Plant Physiol 107:421–427

    PubMed Central  CAS  PubMed  Google Scholar 

  • von Caemmerer S, Evans JR (1991) Determination of the CO2 pressure in chloroplasts from leaves of several C3 plants. Aust J Plant Physiol 18:287–305

    Article  Google Scholar 

  • Wada M (2013) Chloroplast movement. Plant Sci 210:177–182

    Article  CAS  PubMed  Google Scholar 

  • Walker B, Ariza LS, Kaines S, Badger MR, Cousins AB (2013) Temperature response of in vivo Rubisco kinetics and mesophyll conductance in Arabidopsis thaliana: comparisons to Nicotiana tabacum. Plant Cell Environ 36:2108–2119

    Article  CAS  PubMed  Google Scholar 

  • Warren CR (2008) Stand aside stomata, another actor deserves centre stage: the forgotten role of the internal conductance to CO2 transfer. J Exp Bot 59:1475–1487

    Article  CAS  PubMed  Google Scholar 

  • Warren C, Dreyer E (2006) Temperature response of photosynthesis and internal conductance to CO2: results from two independent approaches. J Exp Bot 57:3057–3067

    Article  CAS  PubMed  Google Scholar 

  • Yoder DW, Kadirjan-Kalbach D, Olson BJSC, S-y Miyagishima, DeBlasio SL, Hangarter RP, Osteryoung KW (2007) Effects of mutations in Arabidopsis FtsZ1 on plastid division, FtsZ ring formation and positioning, and FtsZ filament morphology in vivo. Plant Cell Physiol 48:775–791

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Dr. Katherine Osteryoung for providing the arc mutant seeds and for thoughtful discussions throughout the project. This work was supported by DOE grant DE-SC0008509 to TDS and NSF grant IOS-0719118 and NIH grant NIH-NCRR P20RR18754 to DTH. Partial salary support for TDS comes from Michigan State University AgBioResearch.

Author information

Authors and Affiliations

  1. Department of Biochemistry & Molecular Biology, Michigan State University, 603 Wilson Road, Room 201, East Lansing, MI, 48824, USA

    Sean E. Weise, David J. Carr, Ashley M. Bourke, Debbie Swarthout & Thomas D. Sharkey

  2. Department of Biology, University of New Mexico, Albuquerque, NM, USA

    David T. Hanson

Authors
  1. Sean E. Weise
    View author publications

    You can also search for this author inPubMed Google Scholar

  2. David J. Carr
    View author publications

    You can also search for this author inPubMed Google Scholar

  3. Ashley M. Bourke
    View author publications

    You can also search for this author inPubMed Google Scholar

  4. David T. Hanson
    View author publications

    You can also search for this author inPubMed Google Scholar

  5. Debbie Swarthout
    View author publications

    You can also search for this author inPubMed Google Scholar

  6. Thomas D. Sharkey
    View author publications

    You can also search for this author inPubMed Google Scholar

Corresponding author

Correspondence to Thomas D. Sharkey.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 100 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Weise, S.E., Carr, D.J., Bourke, A.M. et al. The arc mutants of Arabidopsis with fewer large chloroplasts have a lower mesophyll conductance. Photosynth Res 124, 117–126 (2015). https://doi.org/10.1007/s11120-015-0110-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-015-0110-4

Keywords