Photosynthetica

, Volume 56, Issue 1, pp 382–391 | Cite as

Tocopherols modulate leaf vein arrangement and composition without impacting photosynthesis

  • J. J. Stewart
  • W. W. Adams
  • C. M. Cohu
  • B. Demmig-Adams
Article

Abstract

Growth of the tocopherol-deficient vte1 mutant and Col-0 wild type of Arabidopsis thaliana in a sunlit glasshouse revealed both similarities and differences between genotypes. Photosynthetic capacity and leaf mesophyll features did not differ between mutant and wild type. Likewise, the total volume of water conduits (tracheary elements, TEs), sugar conduits (sieve elements, SEs), and sugar-loading cells (companion and phloem parenchyma cells) on a leaf area basis were unaffected by tocopherol deficiency. However, tocopherol deficiency yielded smaller and more numerous minor veins with fewer phloem cells and smaller TEs, resulting in greater ratios of TEs to SEs. The smaller TEs in the vte1 mutant may present a decreased risk for cavitation under high evaporative demand or in response to freezing. In turn, compensation for fewer phloem cells and smaller TEs by more numerous veins may bolster resistance to cavitation at no cost to photosynthetic capacity.

Additional key words

foliar vasculature leaf venation vein density vitamin E deficiency xylem 

Abbreviations

CC

companion cell

Chl

chlorophyll

DM

dry mass

PC

phloem parenchyma cell

SE

sieve element

TE

tracheary element

VD

vein density

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 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.PubMedPubMedCentralGoogle Scholar
  2. 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
  3. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  4. 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.CrossRefPubMedGoogle Scholar
  5. Allu A.D., Simancas B., Balazadeh S., Munné-Bosch S.: Defense-related transcriptional reprogramming in vitamin Edeficient Arabidopsis mutants exposed to contrasting phosphate availability.–Front. Plant Sci. 8: 1396, 2017.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 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.CrossRefGoogle Scholar
  7. 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.PubMedPubMedCentralGoogle Scholar
  8. 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.PubMedPubMedCentralGoogle Scholar
  9. 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.CrossRefGoogle Scholar
  10. Considine M.J., Foyer C.H.: Redox regulation of plant development.–Antioxid. Redox Sign. 21: 1305–1326, 2014.CrossRefGoogle Scholar
  11. 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.CrossRefPubMedGoogle Scholar
  12. Demmig-Adams B., Cohu C.M., Muller O., Adams W.W. III: Modulation of photosynthetic energy conversion efficiency in nature: from seconds to seasons.–Photosynth. Res. 113: 75–88, 2012.CrossRefPubMedGoogle Scholar
  13. Demmig-Adams B., Cohu C.M., Amiard V. et al.: Emerging trade-offs–impact of photoprotectants (PsbS, xanthophylls, and vitamin E) on oxylipins as regulators of development and defense.–New Phytol. 197: 720–729, 2013.CrossRefPubMedGoogle Scholar
  14. 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. R. Soc. B 269: 20130244, 2014a.CrossRefGoogle Scholar
  15. Demmig-Adams B., Stewart J.J., Adams W.W. III: Photoprotection and the trade-off between abiotic and biotic defense.–In: Demmig-Adams B., Garab G., Adams W.W. III, Govindjee (ed.): Non-Photochemical Quenching and Energy Dissipation in Plants, Algae and Cyanobacteria. Pp. 631–643. Springer, Dordrecht 2014b.Google Scholar
  16. Demmig-Adams B., Stewart J.J., Burch T.A., Adams W.W. III: Insights from placing photosynthetic light harvesting into context.–J. Phys. Chem. Lett. 5: 2880–2889, 2014c.CrossRefPubMedGoogle Scholar
  17. Delieu T., Walker D.A.: Polarographic measurements of photosynthetic oxygen evolution by leaf discs.–New Phytol. 89: 165–178, 1981.CrossRefGoogle Scholar
  18. 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.CrossRefPubMedGoogle Scholar
  19. Fatichi S., Leuzinger S., Körner C.: Moving beyond photosynthesis: from carbon source to sink-driven vegetation modeling.–New Phytol. 201: 1086–1095, 2014.CrossRefPubMedGoogle Scholar
  20. Foyer C.H., Noctor G.: Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications.–Antioxid. Redox Sign. 11: 861–905, 2009.CrossRefGoogle Scholar
  21. Foyer C.H., Noctor G.: Redox signaling in plants.–Antioxid. Redox Sign. 18: 2087–2090, 2013.CrossRefGoogle Scholar
  22. Gehan M.A., Park S., Gilmour S.J. et al.: Natural variation in the C-repeat binding factor cold response pathway correlates with local adaptation of Arabidopsis ecotypes.–Plant J. 84: 682–693, 2015.CrossRefPubMedGoogle Scholar
  23. Hacke U.G., Sperry J.S.: Functional and ecological xylem anatomy.–Perspect. Plant Ecol. 4: 97–115, 2001.CrossRefGoogle Scholar
  24. Hacke U.G., Jacobsen A.L., Pratt R.B.: Xylem function of aridland shrubs from California, USA: an ecological and evolutionary analysis.–Plant Cell Environ. 32: 1324–1333, 2009.CrossRefPubMedGoogle Scholar
  25. Hargrave K.R., Kolb K.J., Ewers F.W., Davis S.D.: Conduit diameter and drought-induced embolism in Salvia mellifera Greene (Labiatae).–New Phytol. 126: 695–705, 1994.CrossRefGoogle Scholar
  26. Havaux M., García-Plazaola J.I.: Beyond non-photochemical fluorescence quenching: the overlapping antioxidant functions of zeaxanthin and tocopherols.–In: Demmig-Adams B., Garab G., Adams W.W. III, Govindjee (ed.) Non-Photochemical Quenching and Energy Dissipation in Plants, Algae and Cyanobacteria. Pp. 583–603. Springer, Dordrecht 2014.Google Scholar
  27. Hölttä T., Nikinmaa E.: Modelling the effect of xylem and phloem transport on leaf gas exchange.–Acta Hortic. 991: 351–358, 2013.CrossRefGoogle Scholar
  28. Hölttä T., Vesala T., Sevanto S. et al.: Modeling xylem and phloem water flows in trees according to cohesion theory and Münch hypothesis.–Trees 20: 67–78, 2006.CrossRefGoogle Scholar
  29. Hüner N.P.A., Maxwell D.P, Gray G.R. et al.: Sensing environmental temperature change through imbalances between energy supply and energy consumption: redox state of photosystem II.–Physiol. Plantarum 98: 358–364, 1996.CrossRefGoogle Scholar
  30. Hüner N.P.A., Bode R., Dahal K. et al.: Chloroplast redox imbalance governs phenotypic plasticity: the “grand design of photosynthesis” revisited.–Front. Plant Sci. 3: 255, 2012.CrossRefPubMedPubMedCentralGoogle Scholar
  31. Hüner N.P.A., Dahal K., Bode R. et al.: Photosynthetic acclimation, vernalization, crop productivity and the ‘grand design of photosynthesis’.–J. Plant Physiol. 203: 29–43, 2016.CrossRefPubMedGoogle Scholar
  32. Kang J., Dengler N.: Vein pattern development in adult leaves of Arabidopsis thaliana.–Int. J. Plant Sci. 165: 231–242, 2004.CrossRefGoogle Scholar
  33. Kang J., Zhang H., Sun T. et al.: Natural variation of C-repeatbinding factor (CBFs) genes is a major cause of divergence in freezing tolerance among a group of Arabidopsis thaliana populations along the Yangtze River in China.–New Phytol. 199: 1069–1080, 2013.CrossRefPubMedGoogle Scholar
  34. Körner C.: Growth controls photosynthesis–mostly.–Nova Act. Lc. 114: 273–283, 2013.Google Scholar
  35. Ksas B., Becuwe N., Chevalier A., Havaux M.: Plant tolerance to excess light energy and photooxidative damage relies on plastoquinone biosynthesis.–Sci. Rep. 5: 10919, 2015.CrossRefPubMedPubMedCentralGoogle Scholar
  36. Külheim C., Ågren J., Jansson S.: Rapid regulation of light harvesting and plant fitness in the field.–Science 297: 91–93, 2002.CrossRefPubMedGoogle Scholar
  37. Kurepin L.V., Dahal K.P., Savitch L.V. et al.: Role of CBFs as integrators of chloroplast redox, phytochrome and plant hormone signaling during cold acclimation.–Int. J. Mol. Sci. 14: 12729–12763, 2013.CrossRefPubMedPubMedCentralGoogle Scholar
  38. Logan B.A., Kornyeyev D., Hardison J., Holaday A.S.: The role of antioxidant enzymes in photoprotection.–Photosynth. Res. 88: 119–132, 2006.CrossRefPubMedGoogle Scholar
  39. Maeda H., Song W., Sage T.L., DellaPenna D.: Tocopherols play a crucial role in low-temperature adaptation and phloem loading in Arabidopsis.–Plant Cell 18: 2710–2732, 2006.CrossRefPubMedPubMedCentralGoogle Scholar
  40. Maeda H., Song W., Sage T., DellaPenna D.: Role of callose synthases in transfer cell wall development in tocopherol deficient Arabidopsis mutants.–Front. Plant Sci. 5: 46, 2014.PubMedPubMedCentralGoogle Scholar
  41. Mattsson J., Ckurshumova W., Berleth T.: Auxin signaling in Arabidopsis leaf vascular development.–Plant Physiol. 131: 1327–1339, 2003.CrossRefPubMedPubMedCentralGoogle Scholar
  42. Mène-Saffrané L., DellaPenna D.: Biosynthesis, regulation and function of tocochromanols in plants.–Plant Physiol. Bioch. 48: 301–309, 2010.CrossRefGoogle Scholar
  43. Mishra Y., Jänkänpää H.J., Kiss A.Z. et al.: Arabidopsis plants grown in the field and climate chambers significantly differ in leaf morphology and photosystem components.–BMC Plant Biol. 12: 6, 2012.CrossRefPubMedPubMedCentralGoogle Scholar
  44. 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.CrossRefGoogle Scholar
  45. 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.CrossRefGoogle Scholar
  46. Nikinmaa E., Hölttä T., Hari P. et al.: Assimilate transport in phloem sets conditions for leaf gas exchange.–Plant Cell Environ. 36: 655–669, 2013.CrossRefPubMedGoogle Scholar
  47. Oakley C.G., Ågren J., Atchison R.A., Schemske D.W.: QTL mapping of freezing tolerance: links to fitness and adaptive trade-offs.–Mol. Ecol. 23: 4304–4315, 2014.CrossRefPubMedGoogle Scholar
  48. Paul M.J., Driscoll S.P.: Sugar repression of photosynthesis: The role of carbohydrates on signaling nitrogen deficiency through source:sink imbalance.–Plant Cell Environ. 20: 110–116, 1997.CrossRefGoogle Scholar
  49. Paul M.J., Foyer C.H.: Sink regulation of photosynthesis.–J. Exp. Bot. 52: 1383–1400, 2001.CrossRefPubMedGoogle Scholar
  50. Sack L., Holbrook N.M.: Leaf hydraulics.–Annu. Rev. Plant Biol. 57: 361–381, 2006.CrossRefPubMedGoogle Scholar
  51. 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.CrossRefPubMedGoogle Scholar
  52. Sack L., Scoffoni C., McKown A.D. et al.: Developmentally based scaling of leaf venation architecture explains global ecological patterns.–Nat. Commun. 3: 837, 2012.CrossRefPubMedGoogle Scholar
  53. Sack L., Scoffoni C., Johnson D.M. et al.: The anatomical determinants of leaf hydraulic function.–In: Hacke U. (ed.): Functional and Ecological Xylem Anatomy. Pp. 255–271. Springer, Dordrecht 2015.Google Scholar
  54. Sattler S.E., Cahoon E.B., Coughlan S.J., DellaPenna D.: Characterization of tocopherol cyclases from higher plants and cyanobacteria. Evolutionary implications for tocopherol synthesis and function.–Plant Physiol. 132: 2184–2195, 2003.CrossRefPubMedPubMedCentralGoogle Scholar
  55. Sattler S.E., Mène-Saffrané L., Farmer E.E. et al.: Nonenzymatic lipid peroxidation reprograms gene expression and activates defense markers in Arabidopsis tocopherol-deficient mutants.–Plant Cell 18: 3706–3720, 2006.CrossRefPubMedPubMedCentralGoogle Scholar
  56. Scarpella E., Meijer A.H.: Pattern formation in the vascular system of monocot and dicot plant species.–New Phytol. 164: 209–242, 2004.CrossRefGoogle Scholar
  57. Semchuk N.M., Lushak O.V., Falk J. et al.: Inactivation of genes, encoding tocopherol biosynthesis pathway enzymes, results in oxidative stress in outdoor grown Arabidopsis thaliana.–Plant Physiol. Bioch. 47: 384–390, 2009.CrossRefGoogle Scholar
  58. Sterck F.J., Martínez-Vilalta J., Mencuccini M. et al.: Understanding trait interactions and their impacts on growth in Scots pine branches across Europe.–Funct. Ecol. 26: 541–549, 2012.CrossRefGoogle Scholar
  59. 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, 2015.CrossRefPubMedGoogle Scholar
  60. 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.CrossRefPubMedGoogle Scholar
  61. Stewart J.J., Polutchko S.K., Adams W.W. III et al.: Light, temperature and tocopherol status influence foliar vascular anatomy and leaf function Arabidopsis thaliana.–Physiol. Plantarum 160: 98–110, 2017.CrossRefGoogle Scholar

Copyright information

© The Institute of Experimental Botany 2018

Authors and Affiliations

  • J. J. Stewart
    • 1
  • W. W. Adams
    • 1
  • C. M. Cohu
    • 1
  • B. Demmig-Adams
    • 1
  1. 1.Department of Ecology and Evolutionary BiologyUniversity of ColoradoBoulderUSA

Personalised recommendations