Advertisement

Oecologia

pp 1–12 | Cite as

Height-related variations of leaf traits reflect strategies for maintaining photosynthetic and hydraulic homeostasis in mature and old Pinus densiflora trees

  • Wakana Azuma
  • H. Roaki Ishii
  • Takashi Masaki
Physiological ecology - original research

Abstract

Because tree size and age co-vary, it is difficult to separate their effects on growth and physiological function. To infer causes for age-related height-growth decline, we compared various leaf traits between mature (ca. 100 years) and old (ca. 300 years) trees of Pinus densiflora, having similar heights (ca. 30 m) and growing in the same stand. For many leaf traits, mature and old trees showed similar height-related trends reflecting acclimation to height-related hydraulic limitation for maintaining photosynthetic and hydraulic homeostasis. Photosynthetic capacity was constant within crowns of both age-classes, though 4.9–5.4 μmol CO2 m−2 s−1 lower for old than for mature trees. Biochemical acclimation of photosynthesis, allocating more nitrogen to treetop leaves, was observed only for mature trees. Leaf turgor loss point was also constant within crowns of both age-classes with no significant effect of age on leaf hydraulic traits. In mature trees, leaf capacitance increased, while bulk tissue elastic modulus decreased with height, whereas opposite height-related trends were observed for old trees. For both age-classes, leaf mass per area (LMA), transfusion-tissue area, and xylem area all increased with height, but LMA was ca. 30 g m−2 greater for old than for mature trees. In old trees, mesophyll area decreased with height, suggesting anatomical acclimation to height may negatively affect photosynthetic capacity. We inferred that old trees rely more on morphological than biochemical acclimation and that such post-maturational shift in resource allocation could underlie height-growth decline of P. densiflora after reproductive maturity.

Keywords

Height-growth decline Light-acclimation Morphological plasticity Photosynthesis Leaf hydraulics Leaf anatomy 

Notes

Acknowledgements

We thank Yamanashi Forest Management Office of Forestry Agency of Japan for permission to conduct research. We thank to T. Hirano of Kanto Regional Forest Office and Dr. T. Okamoto of FFPRI for sharing information of stand and soil type of our study site. Part of this research was funded by JSPS research fellow (#13J02390) and JSPS Grants in Aid for Scientific Research Kakenhi (#23380085).

Author contribution statement

AW and HRI conceived, designed, implemented the study and wrote the manuscript. MT conducted the stand survey and analyzed stand-level data.

Supplementary material

442_2018_4325_MOESM1_ESM.docx (69 kb)
Supplementary material 1 (DOCX 69 kb)

References

  1. Ambrose AR, Sillett SC, Dawson TE (2009) Effects of tree height on branch hydraulics, leaf structure and gas exchange in California redwoods. Plant Cell Environ 32:743–757.  https://doi.org/10.1111/j.1365-3040.2009.01950.x CrossRefPubMedGoogle Scholar
  2. Azuma W, Ishii HR, Kuroda K, Kuroda K (2016) Function and structure of leaves contributing to increasing water storage with height in the tallest Cryptomeria japonica trees of Japan. Trees 30:141–152.  https://doi.org/10.1007/s00468-015-1283-3 CrossRefGoogle Scholar
  3. Bacelar EA, Correia CM, Moutinho-Pereira JM, Goncalves BC, Lopes JI, Torres-Pereira JMG (2004) Sclerophylly and leaf anatomical traits of five field-grown olive cultivars growing under drought conditions. Tree Physiol 24:233–239CrossRefGoogle Scholar
  4. Bartlett MK, Scoffoni C, Sack L (2012) The determinants of leaf turgor loss point and prediction of drought tolerance of species and biomes: a global meta-analysis. Ecol Lett 15:393–405.  https://doi.org/10.1111/j.1461-0248.2012.01751.x CrossRefPubMedGoogle Scholar
  5. Bartlett MK, Zhang Y, Kreidler N, Sun S, Ardy R, Cao K, Sack L (2014) Global analysis of plasticity in turgor loss point, a key drought tolerance trait. Ecol Lett 17:1580–1590CrossRefGoogle Scholar
  6. Bennett AC, Mcdowell NG, Allen CD, Anderson-Teixeira KJ (2015) Larger trees suffer most during drought in forests worldwide. Nat Plant 28:1–5.  https://doi.org/10.1038/nplants.2015.139 CrossRefGoogle Scholar
  7. Binkley D, Stape JL, Ryan MJ, Barnard HR, Fownes J (2002) Age-related decline in forest ecosystem growth: an individual-tree, stand-structure hypothesis. Ecosystems 5:58–67CrossRefGoogle Scholar
  8. Blackman CJ, Brodribb TJ, Jordan GJ (2009) Leaf hydraulics and drought stress: response, recovery and survivorship in four woody temperate plant species. Plant Cell Environ 32:1584–1595CrossRefGoogle Scholar
  9. Bleby TM, Colquhoun IJ, Adams MA (2012) Hydraulic traits and water use of Eucalyptus on restored versus natural sites in a seasonally dry forest in southwestern Australia. For Ecol Manag 274:58–66.  https://doi.org/10.1016/j.foreco.2012.02.029 CrossRefGoogle Scholar
  10. Bond BJ (2000) Age-related changes in photosynthesis of woody plants. Trends Plant Sci 5:349–353CrossRefGoogle Scholar
  11. Bond BJ, Czarnomski NM, Cooper C, Day ME, Greenwood MS (2007) Developmental decline in height growth in Douglas-fir. Tree Physiol 27:441–453CrossRefGoogle Scholar
  12. Bowman MJS, Brienen RJW, Gloor E, Phillips OL, Prior LD (2013) Detecting trends in tree growth: not so simple. Trends Plant Sci 18:11–17CrossRefGoogle Scholar
  13. Brodribb TJ, Holbrook NM (2005) Water stress deforms tracheids peripheral to the leaf vein of a tropical conifer. Plant Physiol 137:1139–1146CrossRefGoogle Scholar
  14. Brodribb TJ, Holbrook NM, Zwieniecki MA, Palma B (2005) Leaf hydraulic capacity in ferns, conifers and angiosperms: impacts on photosynthetic maxima. New Phytol 165:839–846CrossRefGoogle Scholar
  15. Burgess SSO, Pittermann J, Dawson TE (2006) Hydraulic efficiency and safety of branch xylem increases with height in Sequoia sempervirens (D. Don) crowns. Plant Cell Environ 29:229–239CrossRefGoogle Scholar
  16. Canham CD (1989) Different responses to gaps among shade-tolerant tree species. Ecology 70:548–550CrossRefGoogle Scholar
  17. Chin ARO, Sillett SC (2016) Phenotypic plasticity of leaves enhances water-stress tolerance and promotes hydraulic conductivity in a tall conifer. Am J Bot 103:1–12.  https://doi.org/10.3732/ajb.1600110 CrossRefGoogle Scholar
  18. Chin ARO, Sillett SC (2017) Leaf acclimation to light availability supports rapid growth in tall Picea sitchensis trees. Tree Physiol 37:1352–1366.  https://doi.org/10.1093/treephys/tpx027 CrossRefPubMedGoogle Scholar
  19. Coble AP, Autio A, Cavaleri MA, Binkley D, Ryan MG (2014) Converging patterns of vertical variability in leaf morphology and nitrogen across seven Eucalyptus plantations in Brazil and Hawaii, USA. Trees Struct Funct 28:1–15.  https://doi.org/10.1007/s00468-013-0925-6 CrossRefGoogle Scholar
  20. Coble AP, Cavaleri MA (2015) Light acclimation optimizes leaf functional traits despite height-related constraints in a canopy shading experiment. Oecol 177:1131–1143.  https://doi.org/10.1007/s00442-015-3219-4 CrossRefGoogle Scholar
  21. Coble AP, Cavaleri MA (2017) Vertical leaf mass per area gradient of mature sugar maple reflects both height-driven increases in vascular tissue and light-driven increases in palisade layer thickness. Tree Physiol 37:1337–1351.  https://doi.org/10.1093/treephys/tpx016 CrossRefPubMedGoogle Scholar
  22. Connor KF, Lanner RM (1990) Effects of tree age on secondary xylem and phloem anatomy in stems of Great Basin Bristlecone Pine (Pinus longaeva). Am J Bot 77:1070–1077CrossRefGoogle Scholar
  23. Day ME, Greenwood MS, Diaz-Sala C (2002) Age and size related trends in woody plant shoot development: regulatory pathways and evidence for genetic control. Tree Physiol 22:507–513.  https://doi.org/10.1093/treephys/22.8.507 CrossRefPubMedGoogle Scholar
  24. Day ME, Greenwood MS, White AS (2001) Age-related changes in foliar morphology and physiology in red spruce and their influence on declining photosynthetic rates and productivity with tree age. Tree Physiol 21:1195–1204.  https://doi.org/10.1093/treephys/21.16.1195 CrossRefPubMedGoogle Scholar
  25. England JR, Attiwill PM (2006) Changes in leaf morphology and anatomy with tree age and height in the broadleaved evergreen species, Eucalyptus regnans F. Muell. Trees 20:79–90.  https://doi.org/10.1007/s00468-005-0015-5 CrossRefGoogle Scholar
  26. Gleason SM, Westoby M, Jansen S, Choat B, Hacke UG, Pratt RB, Bhaskar R, Brodribb TJ, Bucci SJ, Cao K-F, Cochard H, Delzon S, Domec J-C, Fan Z-X, Feild TS, Jacobsen AL, Johnson DM, Lens F, Maherali H, Martinez-Vilalta J, Mayr S, McCulloh KA, Mencuccini M, Mitchell PJ, Morris H, Nardini A, Pittermann J, Plavcova L, Schreiber SG, Sperry JS, Wright IJ, Zanne AE (2016) Weak tradeoff between xylem safety and xylem-specific hydraulic efficiency across the world’s woody plant species. New Phytol 209:123–136CrossRefGoogle Scholar
  27. Greenwood MS, Day ME, Schatz J (2010) Separating the effects of tree size and meristem maturation on shoot development of grafted scions of red spruce (Picea rubens Sarg.). Tree Physiol 30:459–468.  https://doi.org/10.1093/treephys/tpq004 CrossRefPubMedGoogle Scholar
  28. Greenwood MS, Ward MH, Day ME, Adams SL, Bond BJ (2008) Age-related trends in red spruce foliar plasticity in relation to declining productivity. Tree Physiol 28:225–232CrossRefGoogle Scholar
  29. Han Q (2011) Height-related decreases in mesophyll conductance, leaf photosynthesis and compensating adjustments associated with leaf nitrogen concentrations in Pinus densiflora. Tree Physiol 31:976–984.  https://doi.org/10.1093/treephys/tpr016 CrossRefPubMedGoogle Scholar
  30. Han Q, Kawasaki T, Nakano T, Chiba Y (2008) Leaf-age effects on seasonal variability in photosynthetic parameters and its relationships with leaf mass per area and leaf nitrogen concentration within a Pinus densiflora crowns. Tree Physiol 28:551–558CrossRefGoogle Scholar
  31. Hinckley TM, Duhme F, Hinckley AR, Richter H (1980) Water relations of drought hardy shrubs: osmotic potential and stomatal reactivity. Plant Cell Environ 3:131–140Google Scholar
  32. Ishii H, Azuma W, Shiraki A, Kuroda K (2017) Hydraulic architecture and function of tall trees. J Jpn For Soc 99:74–83CrossRefGoogle Scholar
  33. Ishii H, Kitaoka S, Fujisaki T, Maruyama Y, Koike T (2007) Plasticity of shoot and needle morphology and photosynthesis of two Picea species with different site preferences in northern Japan. Tree Physiol 27:1595–1605CrossRefGoogle Scholar
  34. Ishii H, Takashima A, Makita N, Yoshida S (2010) Vertical stratification and effects of crown damage on maximum tree height in mixed conifer-broadleaf forests of Yakushima Island, southern Japan. Plant Ecol 211:27–36.  https://doi.org/10.1007/s11258-010-9768-z CrossRefGoogle Scholar
  35. Ishii HR, Azuma W, Kuroda K, Sillett SC (2014) Pushing the limits to tree height: could foliar water storage compensate for hydraulic constraints in Sequoia sempervirens? Funct Ecol 28:1087–1093CrossRefGoogle Scholar
  36. Johnson DM, Meinzer FC, Woodruff DR, McCulloh KA (2009) Leaf xylem embolism, detected acoustically and by cryo-SEM, corresponds to decreases in leaf hydraulic conductance in four evergreen species. Plant Cell Environ 32:828–836.  https://doi.org/10.1111/j.1365-3040.2009.01961.x CrossRefPubMedGoogle Scholar
  37. Koch GW, Sillett SC, Jennings GM, Davis SD (2004) The limits to tree height. Nature 428:851–854CrossRefGoogle Scholar
  38. Kolb TE, Stone JE (2000) Differences in leaf gas exchange and water relations among species and tree sizes in an Arizona pine–oak forest. Tree Physiol 20:1–12CrossRefGoogle Scholar
  39. Kubiske ME, Abrams MD (1991) Rehydration effects on pressure-volume relationships in four temperate woody species: variability with site, time of season and drought conditions. Oecologia 85:537–542CrossRefGoogle Scholar
  40. Kuusk V, Niinemets Ü, Valladares F (2017) A major trade-off between structural and photosynthetic investments operative across plant and needle ages in three mediterranean pines. Tree Physiol 38:543–557.  https://doi.org/10.1093/treephys/tpx139 CrossRefGoogle Scholar
  41. Lanner RM, Connor KF (2001) Does bristlecone pine senesce? Exp Gerontol 36:675–685.  https://doi.org/10.1016/S0531-5565(00)00234-5 CrossRefPubMedGoogle Scholar
  42. Maréchaux I, Bartlett MK, Sack L, Baraloto C, Engel J, Joetzjer E, Chave J (2015) Drought tolerance as predicted by leaf water potential at turgor loss point varies strongly across species within an Amazonian forest. Funct Ecol 29:1268–1277CrossRefGoogle Scholar
  43. Martinez-Vilalta J, Vanderklein D, Mencuccini M (2007) Tree height and age-related decline in growth in Scots pine (Pinus sylvestris L.). Oecol 150:529–544.  https://doi.org/10.1007/s00442-006-0552-7 CrossRefGoogle Scholar
  44. Matsuzaki J, Norisada M, Kodaira J, Suzuki M, Tange T (2005) Shoots grafted into the upper crowns of tall Japanese cedar (Cryptomeria japonica) show foliar gas exchange characteristics similar to those of intact shoots. Trees 19:198–203CrossRefGoogle Scholar
  45. McDill ME, Amateis RL (1992) Measuring forest site quality using the parameters of a dimensionally compatible height growth function. For Sci 38:409–429Google Scholar
  46. McDowell N, Barnard H et al (2002) The relationship between tree height and leaf area: sapwood area ratio. Oecol 132:12–20CrossRefGoogle Scholar
  47. Meinzer FC, McCulloh KA, Lachenbruch B, Woodruff DR, Johnson DM (2010) The blind men and the elephant: the impact of context and scale in evaluating conflicts between plant hydraulic safety and efficiency. Oecol 164:287–296CrossRefGoogle Scholar
  48. Mencuccini M, Martinez-Vilalta J, Hamid HA, Korakaki E, Vanderklein D (2007) Evidence for age- and size-mediated controls of tree growth from grafting studies. Tree Physiol 27:463–473CrossRefGoogle Scholar
  49. Merilo E, Tulva I, Raim O, Kukit A, Sellin A, Kull O (2009) Changes in needle nitrogen partitioning and photosynthesis during 80 years of tree ontogeny in Picea abies. Tree Physiol 23:951–958CrossRefGoogle Scholar
  50. Midgley JJ (2003) Is bigger better in plants? The hydraulic costs of increasing size in trees. Trends Ecol Evol 18:5–6CrossRefGoogle Scholar
  51. Miki N, Otsuki K, Sakamoto K, Nishimoto T, Yoshikawa K (2003) Leaf water relations in Pinus densiflora Sieb. et Zucc. on different soil moisture conditions. J For Res 8:153–161CrossRefGoogle Scholar
  52. Moles AT, Warton DI, Warman L, Swenson NG, Laffan SW, Zanne AE, Pitman A, Hemmings FA, Leishman MR (2009) Global patterns in plant height. J Ecol 97:923–932CrossRefGoogle Scholar
  53. Murty D, Murtrie REMC, Ryan MG (1996) Declining forest productivity in aging forest stands: a modeling analysis of alternative hypotheses. Tree Physiol 16:187–200CrossRefGoogle Scholar
  54. Nardini A, Lo Gullo MA, Salleo S (1999) Competitive strategies for water availability in two mediterranean Quercus species. Plant Cell Environ 22:109–116.  https://doi.org/10.1046/j.1365-3040.1999.00382.x CrossRefGoogle Scholar
  55. Niinemets Ü (2002) Stomatal conductance alone does not explain the decline in foliar photosynthetic rates with increasing tree age and size in Picea abies and Pinus sylvestris. Tree Physiol 22:515–535CrossRefGoogle Scholar
  56. Niinemets Ü (2010) A review of light interception in plant stands from leaf to canopy in different plant functional types and in species with varying shade tolerance. Ecol Res 25:693–714.  https://doi.org/10.1007/s11284-010-0712-4 CrossRefGoogle Scholar
  57. Norman JM, Welles JM, McDermitt DK (1992) Estimating canopy light-use and transpiration efficiencies from leaf measurements. In: Li-Cor Application Note #105. Li-Cor Inc., Lincoln, NEGoogle Scholar
  58. Ogburn RM, Edwards EJ (2012) Quantifying succulence: a rapid, physiologically meaningful metric of plant water storage. Plant Cell Environ 35:1533–1542.  https://doi.org/10.1111/j.1365-3040.2012.02503.x CrossRefPubMedGoogle Scholar
  59. Oldham AR, Sillett SC, Tomescu AMF, Koch GW (2010) The hydrostatic gradient, not light availability, drives height-related variation in Sequoia sempervirens (Cupressaceae) leaf anatomy. Am J Bot 97:1087–1097.  https://doi.org/10.3732/ajb.0900214 CrossRefPubMedGoogle Scholar
  60. Parker WC, Colombo SJ (1995) A critical re-examination of pressure-volume analysis of conifer shoots: comparison of three procedures for generating PV curves on shoots of Pinus resinosa Ait. seedlings. J Exp Bot 46:1701–1709CrossRefGoogle Scholar
  61. Pfautsch S (2016) Hydraulic anatomy and function of trees—basics and critical developments. Curr For Rep 2:236–248.  https://doi.org/10.1007/s40725-016-0046-8 CrossRefGoogle Scholar
  62. Pfautsch S, Aspinwall MJ, Drake JE, Chacon-Doria L, Langelaan RJA, Tissue DT, Tjoelker MG, Lens F (2018) Traits and trade-offs in whole-tree hydraulic architecture along the vertical axis of Eucalyptus grandis. Ann Bot 121:129–141CrossRefGoogle Scholar
  63. Phillips N, Bond BJ, McDowell NG, Ryan MG, Schauer A (2003) Leaf area compounds height-related hydraulic costs of water transport in Oregon White Oak trees. Funct Ecol 17:832–840CrossRefGoogle Scholar
  64. Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta 975:384–394.  https://doi.org/10.1016/S0005-2728(89)80347-0 CrossRefGoogle Scholar
  65. Räim O, Kaurilind E, Hallik L, Merilo E (2012) Why does needle photosynthesis decline with tree height in norway spruce? Plant Biol 14:306–314.  https://doi.org/10.1111/j.1438-8677.2011.00503.x CrossRefPubMedGoogle Scholar
  66. Richardson AD, Berlyn GP, Ashton PMS, Thadani R, Cameron IR (2000) Foliar plasticity of hybrid spruce in relation to crown position and stand age. Can J Bot 78:305–317Google Scholar
  67. Ritchie G, Roden J (1985) Comparison between two methods of generating pressure—volume curves. Plant Cell Environ 8:49–53CrossRefGoogle Scholar
  68. Ryan MG, Phillips N, Bond BJ (2006) The hydraulic limitation hypothesis revisited. Plant Cell Environ 29:367–381CrossRefGoogle Scholar
  69. Ryan MG, Yoder BJ (1997) Hydraulic limits to tree height and tree growth: what keeps trees from growing beyond a certain height? Bioscience 47:235–242.  https://doi.org/10.2307/1313077 CrossRefGoogle Scholar
  70. Schulte PJ, Hinckley TM (1985) A comparison of pressure-volume curve data analysis techniques. J Exp Bot 36:1590–1602CrossRefGoogle Scholar
  71. Sendall KM, Reich PB (2013) Variation in leaf and twig CO2 flux as a function of plant size: a comparison of seedlings, saplings and trees. Tree Physiol 33:713–729.  https://doi.org/10.1093/treephys/tpt048 CrossRefPubMedGoogle Scholar
  72. Shiraki A, Azuma W, Kuroda K, Ishii HR (2017) Physiological and morphological acclimation to height in cupressoid leaves of 100-year-old Chamaecyparis obtusa. Tree Physiol.  https://doi.org/10.1093/treephys/tpw096 CrossRefPubMedGoogle Scholar
  73. Sillett SC, Van Pelt R, Koch GW, Ambrose AR, Carroll AL, Antoine ME, Mifsud BM (2010) Increasing wood production through old age in tall trees. For Ecol Manag 259:976–994CrossRefGoogle Scholar
  74. Sperry JS, Meinzer FC, McCulloh KA (2008) Safety and efficiency conflicts in hydraulic architecture: scaling from tissues to trees. Plant Cell Environ 31:632–645.  https://doi.org/10.1111/j.1365-3040.2007.01765.x CrossRefPubMedGoogle Scholar
  75. Steele MJ, Coutts MP, Yeoman MM (1989) Developmental-changes in Sitka spruce as indexes of physiological age I. Changes in needle morphology. New Phytol 113:367–375CrossRefGoogle Scholar
  76. Steppe K, Niinemets Ü, Teskey RO (2011) Tree size-and age-related changes in leaf physiology and their influence on carbon gain. In: Meinzer FC, Lachenbruch B, Dawson TE (eds) Size- and age-related changes in tree structure and function. Springer, Dordrecht, pp 235–253CrossRefGoogle Scholar
  77. Tyree MT, Hammel HT (1972) The measurement of the turgor pressure and the water relations of plants by the pressure-bomb technique. J Exp Bot 23:267–282CrossRefGoogle Scholar
  78. Wang GG, Marshall PL, Klinka K (1994) Height growth pattern of white spruce in relation to site quality. For Ecol Manag 68:137–147.  https://doi.org/10.1016/0378-1127(94)90041-8 CrossRefGoogle Scholar
  79. Warren CR, Adams MA (2001) Distribution of N, Rubisco and photosynthesis in Pinus pinaster and acclimation to light. Plant Cell Environ 24:597–609.  https://doi.org/10.1046/j.1365-3040.2001.00711.x CrossRefGoogle Scholar
  80. Weiner J, Thomas SC (2001) The nature of tree growth and the “age-related decline in forest productivity”. Oikos 94:347–376CrossRefGoogle Scholar
  81. Williams CB, Reese Naesborg R, Dawson TE, Cavaleri M (2017) Coping with gravity: the foliar water relations of giant sequoia. Tree Physiol 37:1312–1326.  https://doi.org/10.1093/treephys/tpx074 CrossRefPubMedGoogle Scholar
  82. Woodruff DR, Meinzer FC (2011) Size-dependent changes in biophysical control of tree growth: the role of turgor. In: Meinzer FC, Lachenbruch B, Dawson TE (eds) Size- and age-related changes in tree structure and function, Tree physi. Springer, Dordrecht, pp 363–384CrossRefGoogle Scholar
  83. Woodruff DR, Meinzer FC, Lachenbruch B, Johnson DM (2009) Coordination of leaf structure and gas exchange along a height gradient in a tall conifer. Tree Physiol 29:261–272.  https://doi.org/10.1093/treephys/tpn024 CrossRefPubMedGoogle Scholar
  84. Xu C-Y, Turnbull MH, Tissue DT, Lewis JD, Carson R, Schuster WSF, Whitehead D, Walcroft AS, Li J, Griffin KL (2012) Age-related decline of stand biomass accumulation is primarily due to mortality and not to reduction in NPP associated with individual tree physiology, tree growth or stand structure in a Quercus-dominated forest. J Ecol 100:428–440CrossRefGoogle Scholar
  85. Zhang Y-J, Rockwell FE, Wheeler JK, Holbrook NM (2014) Reversible deformation of transfusion tracheids in Taxus baccata is associated with a reversible decrease in leaf hydraulic conductance. Plant Physiol 165:1557–1565.  https://doi.org/10.1104/pp.114.243105 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Graduate School of AgricultureKyoto UniversityKyotoJapan
  2. 2.Graduate School of Agricultural ScienceKobe UniversityKobeJapan
  3. 3.Forestry and Forest Products Research Institute (FFPRI)TsukubaJapan

Personalised recommendations