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Evaluating the link between photosynthetic capacity and leaf vascular organization with principal component analysis

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Photosynthetica

Abstract

Significant linear relationships between photosynthetic capacity and principal components loaded by phloem cell numbers and tracheary elements per minor vein as well as the latter two normalized for vein density (proxy for apoplastic phloem loading capacity involving membrane transporters) were revealed for all apoplastic loaders (summer annuals and winter annual Arabidopsis thaliana). In addition, significant linear relationships between photosynthetic capacity and a principal component loaded by tracheary element cross-sectional areas and volumes per unit of leaf area (water flux capacity proxy) was present for symplastic and apoplastic loaders. Lastly, a significant linear relationship between photosynthetic capacity and a principal component loaded by phloem cell cross-sectional areas and volumes per unit of leaf area (proxy for symplastic loading capacity involving cytosolic enzymes for companion cells) was revealed for summer annual symplastic loaders as well as for A. thaliana (in the case of sieve elements, a proxy for sugar export capacity from the leaves).

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Abbreviations

CC:

companion cell

LC:

loading cell (i.e., CC and PPC)

PC:

principal component

PCA:

principal component analysis

PPC:

phloem parenchyma cell

SA:

summer annual

SE:

sieve element

TE:

tracheary element

VD:

vein density

References

  • Abdi H., Williams L.J.: Principal component analysis.–WIRESComput. Stat. 2: 433–459, 2010.

    Google Scholar 

  • Adams W.W. III, Amiard V.S.E., Mueh K.E. et al.: Phloem loading type and photosynthetic acclimation to light.–In: van der Est A., Bruce D. (ed.): Photosynthesis: Fundamental Aspects to Global Perspectives. Pp. 814–816. Allen Press, Lawrence 2005.

    Google Scholar 

  • Adams W.W. III, Cohu C.M., Amiard V., Demmig-Adams B.: Associations between phloem-cell wall ingrowths in minor veins and maximal photosynthesis rate.–Front. Plant Sci. 5: 24, 2014.

    Google Scholar 

  • Adams W.W. III, Muller O., Cohu C.M., Demmig-Adams B.: Foliar phloem infrastructure in support of photosynthesis.–Front. Plant Sci. 4: 194, 2013.

    PubMed  PubMed Central  Google Scholar 

  • Adams W.W. III, Stewart J.J., Cohu C.M. et al.: Habitat temperature and precipitation of Arabidopsis thaliana ecotypes determine the response of foliar vasculature, photosynthesis, and transpiration to growth temperature.–Front. Plant Sci. 7: 1026, 2016.

    Article  PubMed  PubMed Central  Google Scholar 

  • Adams W.W. III, Watson A.M., Mueh K.E. et al.: Photosynthetic acclimation in the context of structural constraints to carbon export from leaves.–Photosynth. Res. 94: 455–466, 2007

    Article  PubMed  CAS  Google Scholar 

  • Ågren J., Schemske D.W.: Reciprocal transplants demonstrate strong adaptive differentiation of the model organism Arabidopsis thaliana in its native range.–New Phytol. 194: 1112–1122, 2012.

    Article  PubMed  Google Scholar 

  • Amiard V., Mueh K.E., Demmig-Adams B. et al.: Role of light and jasmonic acid signaling in regulating foliar phloem cell wall ingrowth development.–New Phytol. 173: 722–731, 2007.

    Article  PubMed  CAS  Google Scholar 

  • Amiard V., Mueh K.E., Demmig-Adams B. et al: Anatomical and photosynthetic acclimation to the light environment in species with differing mechanisms of phloem loading.–P. Natl. Acad. Sci. USA 102: 12968–12973, 2005.

    Article  CAS  Google Scholar 

  • Beerling D.J., Franks P.J: The hidden cost of transpiration.–Nature 464: 495–496, 2010.

    Article  PubMed  CAS  Google Scholar 

  • Beikircher B., Mittmann C., Mayr S.: Prolonged soil frost affects hydraulics and phenology of apple trees.–Front. Plant Sci. 7: 867, 2016.

    Article  PubMed  PubMed Central  Google Scholar 

  • Blonder B., Violle C., Bentley L.P., Enquist B.J.: Venation networks and the origin of the leaf economics spectrum.–Ecol. Lett. 14: 91–100, 2011.

    Article  PubMed  Google Scholar 

  • Bond B.J., Kavanagh K.L.: Stomatal behavior of four woody species in relation to leaf-specific hydraulic conductance and threshold water potential.–Tree Physiol. 19: 503–510, 1999.

    Article  PubMed  Google Scholar 

  • Boyce C.K., Brodribb T.J., Feild T.S., Zwieniecki M.A.: Angiosperm leaf vein evolution was physiologically and environmentally transformative.–Philos. T. Roy. Soc. B-Biol. Sci. 276: 1771–1776, 2009.

    Article  Google Scholar 

  • Brodribb T.J., Feild T.S., Jordan G.J.: Leaf maximum photosynthetic rate and venation are linked by hydraulics.–Plant Physiol. 144: 1890–1898, 2007.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Brodribb T.J., Feild T.S., Sack L.: Viewing leaf structure and evolution from a hydraulic perspective.–Funct. Plant Biol. 37: 488–498, 2010.

    Article  Google Scholar 

  • Brodribb T.J., Feild T.S.: Leaf hydraulic evolution led a surge in leaf photosynthetic capacity during early angiosperm diversification.–Ecol. Lett. 13: 175–183, 2010.

    Article  PubMed  Google Scholar 

  • Brodribb T.J., Holbrook N.M., Zwieniecki M.A., Palma B.: Leaf hydraulic capacity in ferns, conifers and angiosperms: impacts on photosynthetic maxima.–New Phytol. 165: 839–846, 2005.

    Article  PubMed  Google Scholar 

  • Brodribb T.J., Jordan G.J.: Internal coordination between hydraulics and stomatal control in leaves.–Plant Cell Environ. 31: 1557–1564, 2008.

    Article  PubMed  Google Scholar 

  • Brodribb T.J.: Xylem hydraulic physiology: The functional backbone of terrestrial plant productivity.–Plant Sci. 177: 245–251, 2009.

    Article  CAS  Google Scholar 

  • Cavender-Bares J., Cortes P., Rambal S. et al.: Summer and winter sensitivity of leaves and xylem to minimum freezing temperatures: a comparison of co-occurring Mediterranean oaks that differ in leaf lifespan.–New Phytol. 168: 597–612, 2005.

    Article  PubMed  CAS  Google Scholar 

  • Cohu C.M., Muller O., Adams W.W. III, Demmig-Adams B.: Leaf anatomical and photosynthetic acclimation to cool temperature and high light in two winter versus summer annuals.–Physiol. Plantarum 152: 164–173, 2014.

    Article  CAS  Google Scholar 

  • Cohu C.M., Muller O., Demmig-Adams B., Adams W.W. III: Minor loading vein acclimation for three Arabidopsis thaliana ecotypes in response to growth under different temperature and light regimes.–Front. Plant Sci. 4: 240, 2013b.

    PubMed  PubMed Central  Google Scholar 

  • Cohu C.M., Muller O., Stewart J.J. et al: Association between minor loading vein architecture and light- and CO2-saturated oxygen evolution among Arabidopsis thaliana ecotypes from different latitudes.–Front. Plant Sci. 4: 264, 2013a.

    PubMed  PubMed Central  Google Scholar 

  • Davis S.D., Sperry J.S., Hacke U.G.: The relationship between xylem conduit diameter and cavitation caused by freezing.–Am. J. Bot. 86: 1367–1372, 1999.

    Article  PubMed  CAS  Google Scholar 

  • Delieu T., Walker D.A.: Polarographic measurements of photosynthetic oxygen evolution by leaf discs.–New Phytol. 89: 165–178, 1981.

    Article  CAS  Google Scholar 

  • Demmig-Adams B., Stewart J.J., Adams W.W. III: Environmental regulation of intrinsic photosynthetic capacity: an integrated view.–Curr. Opin. Plant Biol. 37: 34–41, 2017.

    Article  PubMed  CAS  Google Scholar 

  • Demmig-Adams B., Stewart J.J., Adams W.W. III: Multiple feedbacks between chloroplast and whole plant in the context of plant adaptation and acclimation to the environment.–Philos. T. Roy. Soc. B 369: 20130244, 2014.

    Article  Google Scholar 

  • Dumlao M.R., Darehshouri A., Cohu C.M. et al.: Low temperature acclimation of photosynthetic capacity and leaf morphology in the context of phloem loading type.–Photosynth. Res. 113: 181–189, 2012.

    Article  PubMed  CAS  Google Scholar 

  • Evans J.R., Kaldenhoff R., Genty B., Terashima I.: Resistances along the CO2 diffusion pathway inside leaves.–J. Exp. Bot. 60: 2235–2248, 2009.

    Article  PubMed  CAS  Google Scholar 

  • Fedriani J.M., Garrote P.J., Delgado M.d.M., Penteriani V.: Subtle gardeners: inland predators enrich local topsoils and enhance plant growth.–PLoS ONE 10: e0138273, 2015.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fondy B.R., Geiger D.R.: Sugar selectivity and other characteristics of phloem loading in Beta vulgaris L.–Plant Physiol. 59: 953–960, 1977.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Franks P.J.: Higher rates of leaf gas exchange are associated with higher leaf hydrodynamic pressure gradients.–Plant Cell Environ. 29: 584–592, 2006

    Article  PubMed  Google Scholar 

  • Geiger D.: Plant sucrose transporters from a biophysical point of view.–Mol. Plant. 4: 395–406, 2011.

    Article  PubMed  CAS  Google Scholar 

  • Giaquinta R.T.: Phloem loading of sucrose.–Annu. Rev. Plant Physio. 34: 347–387, 1983.

    Article  CAS  Google Scholar 

  • Gifford R.M., Evans L.T.: Photosynthesis, carbon partitioning, and yield.–Ann. Rev. Plant Physiol. 32: 485–509, 1981.

    Article  CAS  Google Scholar 

  • Gifford R.M., Thorne J.H., Hitz W.D., Gianquinta R.T.: Crop productivity and photoassimilate partitioning.–Science 225: 801–808, 1984.

    Article  PubMed  CAS  Google Scholar 

  • Gorsuch P.A., Pandey S., Atkin O.K.: Temporal heterogeneity of cold acclimation phenotypes in Arabidopsis leaves.–Plant Cell Environ. 33: 244–258, 2010.

    Article  PubMed  CAS  Google Scholar 

  • Hacke U.G., Sperry J.S.: Functional and ecological xylem anatomy.–Perspect. Plant Ecol. 4: 97–115, 2001.

    Article  Google Scholar 

  • Hubbard R.M., Ryan M.G., Stiller V., Sperry J.S.: Stomatal conductance and photosynthesis vary linearly with plant hydraulic conductance in ponderosa pine.–Plant Cell Environ. 24: 113–121, 2001.

    Article  Google Scholar 

  • Jumrani K., Bhatia V.S., Pandey G.P.: Impact of elevated temperatures on specific leaf weight, stomatal density, photosynthesis and chlorophyll fluorescence in soybean.–Photosynth. Res. 131: 333–350, 2017.

    Article  PubMed  CAS  Google Scholar 

  • Klepek Y.S., Geiger D., Stadler R. et al.: Arabidopsis POLYOL TRANSPORTER5, a new member of the monosaccharide transporter-like superfamily, mediates H+-symport of numerous substrates, including myo-inositol, glycerol, and ribosele.–Plant Cell 17: 204–218, 2005.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Koornneef M., Meinke D.: The development of Arabidopsis as a model plant.–Plant J. 61: 909–921, 2010.

    Article  PubMed  CAS  Google Scholar 

  • Kundu S.K, Tigerstedt P.M.A.: Variation in net photosynthesis, stomatal characteristics, leaf area and whole-plant phytomass production among ten provenances of neem (Azadirachta indica).–Tree Physiol. 19: 47–52, 1999.

    Article  PubMed  Google Scholar 

  • Langan S.J., Ewers F.W., Davis S.D.: Xylem dysfunction caused by water stress and freezing in two species of co-occurring chaparral shrubs.–Plant Cell Environ. 20: 425–437, 1997.

    Article  Google Scholar 

  • Liesche J., Schulz A.: Modeling the parameters for plasmodesmal sugar filtering in active symplasmic phloem loaders.–Front. Plant Sci. 4: 207, 2013.

    Article  PubMed  PubMed Central  Google Scholar 

  • Maherali H., Sherrard M.E., Clifford M.H., Latta R.G.: Leaf hydraulic conductivity and photosynthesis are genetically correlated in an annual grass.–New Phytol. 180: 240–247, 2008.

    Article  PubMed  CAS  Google Scholar 

  • McKown A.D., Cochard H., Sack L.: Decoding leaf hydraulics with a spatially explicit model: Principles of venation architecture and implications for its evolution.–Am. Nat. 175: 447–460, 2010.

    Article  PubMed  Google Scholar 

  • Muller O., Cohu C.M., Stewart J.J. et al: Association between photosynthesis and contrasting features of minor veins in leaves of summer annuals loading phloem via symplastic versus apoplastic routes.–Physiol. Plantarum 152: 174–183, 2014a.

    Article  CAS  Google Scholar 

  • Muller O., Stewart J.J., Cohu C.M. et al: Leaf architectural, vascular, and photosynthetic acclimation to temperature in two biennials.–Physiol. Plantarum 152: 763–772, 2014b.

    Article  CAS  Google Scholar 

  • Nardini A., Gortan E., Salleo S.: Hydraulic efficiency of the leaf venation system in sun- and shade-adapted species.–Funct. Plant Biol. 32: 953–961, 2005.

    Article  Google Scholar 

  • Oguchi R., Hikosaka K., Hirose T.: Leaf anatomy as a constraint for photosynthetic acclimation: differential responses in leaf anatomy to increasing growth irradiance among three deciduous species.–Plant Cell Environ. 28: 916–927, 2005.

    Article  Google Scholar 

  • Oguchi R., Hikosaka K., Hiura T., Hirose T.: Costs and benefits of photosynthetic light acclimation by tree seedlings in response to gap formation.–Oecologia 155: 665–675, 2008.

    Article  PubMed  CAS  Google Scholar 

  • Oguchi R., Hikosaka K., Hiura T., Hirose T.: Leaf anatomy and light acclimation in woody seedlings after gap formation in a cool-temperate deciduous forest.–Oecologia 149: 571–582, 2006.

    Article  PubMed  CAS  Google Scholar 

  • Prado K., Maurel C.: Regulation of leaf hydraulics: from molecular to whole plant levels.–Front. Plant Sci. 4: 255, 2013.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pratt R.B., Jacobsen A.L.: Conflicting demands on angiosperm xylem: tradeoffs among storage, transport and biomechanics.–Plant Cell Environ. 40: 897–913, 2017.

    Article  PubMed  CAS  Google Scholar 

  • Provart N.J., Alonso J., Assmann S.M. et al.: 50 years of Arabidopsis research: highlights and future directions.–New Phytol. 209: 921–944, 2016.

    Article  PubMed  CAS  Google Scholar 

  • Ramsperger-Gleixner M., Geiger D., Hedrich R., Sauer N.: Differential expression of sucrose transporter and polyol transporter genes during maturation of common plantain companion cells.–Plant Physiol. 134: 147–160, 2004.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rennie E.A., Turgeon R.: A comprehensive picture of phloem loading strategies.–P. Natl. Acad. Sci. USA 106: 14162–14167, 2009.

    Article  Google Scholar 

  • Repo T., Kalliokoski T., Domisch T. et al: Effects of timing of soil frost thawing on Scots pine.–Tree Physiol. 25: 1053–1062, 2005.

    Article  PubMed  Google Scholar 

  • Repo T., Lehto T., Finér L.: Delayed soil thawing affects root and shoot functioning and growth in Scots pine.–Tree Physiol. 28: 1583–1591, 2008.

    Article  PubMed  Google Scholar 

  • Sack L., Holbrook N.M.: Leaf hydraulics.–Annu. Rev. Plant Biol. 57: 361–381, 2006.

    Article  PubMed  CAS  Google Scholar 

  • Sack L., Scoffoni C.: Leaf venation: structure, function, development, evolution, ecology and applications in the past, present and future.–New Phytol. 198: 983–1000, 2013.

    Article  PubMed  Google Scholar 

  • Santiago L.S., Goldstein G., Meinzer F.C. et al.: Leaf photosynthetic traits scale with hydraulic conductivity and wood density in Panamanian forest canopy trees.–Oecologia 140: 543–550, 2004.

    Article  PubMed  CAS  Google Scholar 

  • Schulz A.: Diffusion or bulk flow: how plasmodesmata facilitate pre-phloem transport of assimilates.–J. Plant Res. 128: 49–61, 2015.

    Article  PubMed  CAS  Google Scholar 

  • Slewinski T.L., Zhang C., Turgeon R.: Structural and functional heterogeneity in phloem loading and transport.–Front. Plant Sci. 4: 244, 2013.

    PubMed  PubMed Central  Google Scholar 

  • Sperry J.S., Hacke U.G., Pitterman J.: Size and function in conifer tracheids and angiosperm vessels.–Am. J. Bot. 93: 1490–1500, 2006.

    Article  PubMed  Google Scholar 

  • Spurr A.R.: A low-viscosity epoxy resin embedding medium for electron microscopy.–J. Ultrastruct. Res. 26: 31–43, 1969.

    Article  PubMed  CAS  Google Scholar 

  • Stewart J.J., Adams W.W. III, Cohu C.M. et al.: Differences in light-harvesting, acclimation to growth-light environment, and leaf structural development between Swedish and Italian ecotypes of Arabidopsis thaliana.–Planta 242: 1277–1290, 20

    Article  PubMed  CAS  Google Scholar 

  • Stewart J.J., Demmig-Adams B., Cohu C.M. et al.: Growth temperature impact on leaf form and function in Arabidopsis thaliana ecotypes from northern and southern Europe.–Plant Cell Environ. 39: 1549–1558, 2016.

    Article  PubMed  CAS  Google Scholar 

  • Stewart J.J., Polutchko S.K., Adams W.W. III et al.: Light, temperature, and tocopherol status influence foliar vascular anatomy and leaf function in Arabidopsis thaliana.–Physiol. Plantarum 160: 98–110, 20

    Article  CAS  Google Scholar 

  • Stewart J.J., Polutchko S.K., Adams W.W. III, Demmig-Adams B.: Acclimation of Swedish and Italian ecotypes of Arabidopsis thaliana to light intensity.–Photosynth. Res.: DOI:10.1007/s11120-017-0436-1, in press, 2017.

    Google Scholar 

  • Strand Å., Hurry V., Gustafsson P., Gardeström P.: Development of Arabidopsis thaliana leaves at low temperature releases the suppression of photosynthesis and photosynthetic gene expression despite the accumulation of soluble carbohydrates.–Plant J. 12: 605–614, 1997.

    Article  PubMed  CAS  Google Scholar 

  • Strand Å., Hurry V., Henkes S. et al.: Acclimation of Arabidopsis leaves developing at low temperatures. Increasing cytoplasmic volume accompanies increased activities of enzymes in the Calvin cycle and in the source-biosynthesis pathway.–Plant Physiol. 119: 1387–1397, 1999.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tanaka Y., Sugano S.S., Shimada T., Hara-Nishimura I.: Enhancement of leaf photosynthetic capacity through increased stomatal density in Arabidopsis.–New Phytol. 198: 757–764, 2013.

    Article  PubMed  CAS  Google Scholar 

  • Taylor S.H., Franks P.J., Hulme S.P. et al.: Photosynthetic pathway and ecological adaptation explain stomatal trait diversity amongst grasses.–New Phytol. 193: 387–396, 2012.

    Article  PubMed  CAS  Google Scholar 

  • Terashima I. Hanba Y.T., Tholen D., Niinemets ü.: Leaf functional anatomy in relation to photosynthesis.–Plant Physiol. 155: 108–116, 2011.

    Article  PubMed  CAS  Google Scholar 

  • Terashima I., Hanba Y.T., Tazoe Y. et al.: Irradiance and phenotype: comparative eco-development of sun and shade leaves in relation to photosynthetic CO2 diffusion.–J. Exp. Bot. 57: 343–354, 2006.

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Walls R.L.: Angiosperm leaf vein patterns are linked to leaf functions in global-scale data set.–Am. J. Bot. 98: 244–253, 2011.

    Article  PubMed  Google Scholar 

  • Wang J., Lu W., Tong Y.X., Yang Q.C.: Leaf morphology, photosynthetic performance, chlorophyll fluorescence, stomatal development of lettuce (Lactuca sativa L.) exposed to different ratios of red light to blue light.–Front. Plant Sci. 7: 250, 2016.

    PubMed  PubMed Central  Google Scholar 

  • Wardlaw I.F.: The control of carbon partitioning in plants.–New Phytol. 116: 341–381, 1990.

    Article  CAS  Google Scholar 

  • Wu B.-J., Chow W.S., Liu Y.-J. et al.: Effects of stomatal development on stomatal conductance and on stomatal limitation of photosynthesis in Syringa oblata and Euonymus japonicas Thunb.–Plant Sci. 229: 23–31, 2014.

    Article  PubMed  CAS  Google Scholar 

  • Zhu S.-D., Song J.-J., Li R.-H., Ye Q.: Plant hydraulics and photosynthesis of 34 woody species from different successional stages of subtropical forests.–Plant Cell Environ. 36: 879–891, 2013.

    Article  PubMed  CAS  Google Scholar 

  • Zimmerman M.H.: Xylem Structure and the Ascent of Sap. Pp. 143. Springer, Berlin 1983.

    Book  Google Scholar 

  • Zweifel R., Steppe K., Sterck F.J.: Stomatal regulation by microclimate and tree water relations: interpreting ecophysiological field data with a hydraulic plant model.–J. Exp. Bot. 58: 2113–2131, 2007.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO, 80309-0334, USA

    S. K. Polutchko, J. J. Stewart, B. Demmig-Adams & W. W. Adams

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  1. S. K. Polutchko
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  2. J. J. Stewart
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  3. B. Demmig-Adams
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Correspondence to W. W. Adams.

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Acknowledgements: We thank Profs. Doug Schemske and Jon Ågren for providing seed of the Italian and Swedish ecotypes of A. thaliana, the USDA GRIN for providing seed of the wild H. annuus, Drs. Christopher Cohu and Onno Muller for data collection, and Dr. Stacey Smith, Dr. Samuel Flaxman, and Mr. Blake Stevison for valuable discussion. This work was supported by the National Science Foundation (Award Number DEB-1022236 to BD-A and WWA) and the University of Colorado at Boulder.

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Polutchko, S.K., Stewart, J.J., Demmig-Adams, B. et al. Evaluating the link between photosynthetic capacity and leaf vascular organization with principal component analysis. Photosynthetica 56, 392–403 (2018). https://doi.org/10.1007/s11099-017-0764-6

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