Skip to main content
Log in

Elevational adaptation of morphological and anatomical traits by Sakhalin fir (Abies sachalinensis)

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

Abstract

Key message

In Sakhalin fir trees from nine different source elevation provenances, we found genetic differentiation of traits related to mechanical reinforcement, hydraulic efficiency, and photosynthetic capacity.

Abstract

Climatic conditions change with elevation and trees must cope with the resulting variation in stresses. Thus, trees may differentiate into elevational ecotypes with genetic-based variations in morphological and physiological traits. To explore genetically differentiated traits related to elevational adaptation, needles and stems were analyzed in 43-year-old Sakhalin fir [Abies sachalinensis (Fr. Schm.) Masters] trees which derived from nine source elevations (230–1250 m above sea level) and grown in a nursery plantation at 230 m above sea level. Trees from a high-elevation provenance showed greater mechanical reinforcement in needles and stems. Needles from high-elevation provenances were shorter and thicker, and developed more sclerenchyma in transfusion tissue. Shorter and thicker stems and larger reaction wood portions were also found. Moreover, needles and stems from high-elevation provenance trees also exhibited xylem traits associated with higher hydraulic efficiency and lower hydraulic safety. In the midrib xylem, the theoretical conductivity was greater due to higher number of tracheids. Pit architecture of stem-xylem tracheid indicated a higher hydraulic efficiency, but lower hydraulic safety due to larger pit apertures. Furthermore, high-elevation provenance trees exhibited a thicker bark, which may reduce water losses and act as a water reservoir in winter. Leaf nitrogen content and stomata number per needle were higher in high-elevation provenance trees, both of which were related to high photosynthetic capacity. Overall, the data suggested genetic differentiation of traits related to various trade-offs and optimization for mechanical resistance, hydraulic efficiency, and photosynthetic capacity at high elevation in Sakhalin fir.

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

Access this article

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

Similar content being viewed by others

References

  • Aitken SN, Hannerz M (2001) Genecology and gene management strategies for conifer cold hardiness. In: Bigras FJ, Columbo SJ (eds) Conifer cold hardiness. Kluwer, Dordrecht, pp 22–53

    Google Scholar 

  • Benomar L, Lamhamedi MS, Rainville A, Beaulieu J, Bousquet J, Margolis HA (2016) Genetic adaptation vs. ecophysiological plasticity of photosynthetic-related traits in young Picea glauca trees along regional climatic gradient. Front Plant Sci 7:48

    Article  PubMed  PubMed Central  Google Scholar 

  • Blackman CJ, Brodribb TJ, Jordan GJ (2010) Leaf hydraulic vulnerability is related to conduit dimensions and drought resistance across a diverse range of woody angiosperms. New Phytol 188:1113–1123

    Article  PubMed  Google Scholar 

  • Bouche PS, Larter M, Domec JC, Burlett R, Gasson P, Jansen S, Delzon S (2014) A broad survey of hydraulic and mechanical safety in the xylem of conifers. J Exp Bot 65:4419–4431

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boyce RL, Lucero SA (1999) Role of roots in winter water relations of Engelmann spruce saplings. Tree Physiol 19:893–898

    Article  CAS  PubMed  Google Scholar 

  • Bressson CC, Vitasse Y, Kremer A, Delzon S (2011) To what extent is altitudinal variation of functional traits driven by genetic adaptation in European oak and beech? Tree Physiol 31:1164–1174

    Article  CAS  Google Scholar 

  • Brodribb TJ, Holbrook NM (2005) Water stress deforms tracheids peripheral to the leaf vein of a tropical conifer. Plant Physiol 137:1139–1146

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cochard H, Froux F, Mayr S, Coutand C (2004) Xylem wall collapse in water-stressed pine needles. Plant Physiol 134:401–408

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • David-Schwartz R, Paudel I, Mizrachi M, Delzon S, Cochard H, Lukyanov V et al (2016) Indirect evidence for genetic differentiation in vulnerability to embolism in Pinus halepensis. Front Plant Sci 7:768

    Article  PubMed  PubMed Central  Google Scholar 

  • Delzon S, Douthe C, Sala A, Cochard H (2010) Mechanism of water-stress induced cavitation in conifers: bordered pit structure and function support the hypothesis of seal capillary-seeding. Plant Cell Environ 33:2101–2111

    Article  PubMed  PubMed Central  Google Scholar 

  • Eiga S, Sakai A (1984) Altitudinal variation in freezing resistance of Sakhalin fir (Abies sachalinensis). Can J Bot 62:156–160

    Article  Google Scholar 

  • Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C-3 plants. Oecologia 78:9–19

    Article  PubMed  Google Scholar 

  • Gardiner B, Berry P, Moulia B (2016) Review: Wind impacts on plant growth, mechanics and damage. Plant Sci 245:94–118

    Article  CAS  PubMed  Google Scholar 

  • Groover A (2016) Gravitropisms and reaction woods of forest trees—evolution, functions and mechanisms. New Phytol 211:790–802

    Article  PubMed  Google Scholar 

  • Hacke UG, Jansen S (2009) Embolism resistance of three boreal conifer species varies with pit structure. New Phytol 182:675–686

    Article  PubMed  Google Scholar 

  • Hacke UG, Sperry JS, Pittermann J (2004) Analysis of circular bordered pit function—II. Gymnosperm tracheids with torus-margo pit membranes. Am J Bot 91:386–400

    Article  PubMed  Google Scholar 

  • Howe GT, Aitken SN, Neale DB, Jermstad KD, Wheeler NC, Chen THH (2003) From genotype to phenotype: unraveling the complexities of cold adaptation in forest trees. Can J Bot 81:1247–1266

    Article  CAS  Google Scholar 

  • Hu YS, Yao BJ (1981) Transfusion tissue in gymnosperm leaves. Bot J Linn Soc 83:263–272

    Article  Google Scholar 

  • 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 28:1087–1093

    Article  Google Scholar 

  • Ishizuka W, Goto S (2012) Modeling intraspecific adaptation of Abies sachaliensis to local altitude and responses to global warming, based on a 36-year reciprocal transplant experiment. Evol App 5:229–244

    Article  Google Scholar 

  • Ishizuka W, Ono K, Hara T, Goto S (2015) Use of intraspecific variation in thermal responses for estimating an elevational cline in the timing of cold hardening in a sub-boreal conifer. Plant Biol 17:177–185

    Article  CAS  PubMed  Google Scholar 

  • Jaffe MJ, Forbes S (1993) Thigmomorphogenesis: the effect of mechanical perturbation on plants. Plant Growth Regul 12:313–324

    Article  CAS  PubMed  Google Scholar 

  • Jones HG (2013) Plants and microclimate: a quantitative approach to environmental plant physiology. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Körner C (2003) Alpine plant life—functional plant ecology of high mountain ecosystems. Springer, Berlin

    Google Scholar 

  • Kouwenberg LLR, Kurschner WM, Visscher H (2004) Changes in stomatal frequency and size during elongation of Tsuga heterophylla needles. Ann Bot 94:561–569

    Article  PubMed  PubMed Central  Google Scholar 

  • Kuhn M (2012) Rain and snow at high elevation: the interaction of water, energy and trace substances. In: Lutz C (ed) Plants in alpine regions. Springer, Wien, pp 1–10

    Google Scholar 

  • Kurahashi A, Hamaya M (1981) Variation of morphological characters and growth response of Sakhalin fir (Abies sachalinensis) in different altitudes. Bull Tokyo Univ For 71:101–151 (in Japanese with English summary)

    Google Scholar 

  • Lamy J, Delzon S, Bouche PS, Alia R, Vendramin GG, Cochard H et al (2014) Limited genetic variability and phenotypic plasticity detected for cavitation resistance in mediterranean pine. New Phytol 201:874–886

    Article  PubMed  Google Scholar 

  • Laur J, Hacke UG (2014) Exploring aquaporins in the context of needle water uptake and xylem refilling. New Phytol 203:388–400

    Article  CAS  PubMed  Google Scholar 

  • Lewis AM, Boose ER (1995) Estimating volume flow-rates through xylem conduits. Am J Bot 82:1112–1116

    Article  Google Scholar 

  • López R, Cano FJ, Choat B, Cochard H, Gil L (2016) Plasticity in vulnerability to cavitation of Pinus canariensis occurs only at the driest end of an aridity gradient. Front Plant Sci 7:769

    Article  PubMed  PubMed Central  Google Scholar 

  • Losso A, Anfodillo T, Ganthaler A, Kofler W, Markl Y, Nardini A, Oberhuber W, Purin G, Mayr S (2018) Robustness of xylem properties in conifers: analyses of tracheid and pit dimensions along elevational transects. Tree Physiol 38:212–222

    Article  PubMed  Google Scholar 

  • Makino A (2003) Rubisco and nitrogen relationships in rice: leaf photosynthesis and plant growth. Soil Sci Plant Nutr 49:319–327

    Article  CAS  Google Scholar 

  • Mayr S, Charra-Vaskou K (2007) Winter at the alpine timberline causes complex within-tree patterns of water potential and embolism in Picea abies. Physiol Plant 131:131–139

    Article  CAS  PubMed  Google Scholar 

  • Mayr S, Cochard H (2003) A new method for vulnerability analysis of small xylem areas reveals that compression wood of Norway spruce has lower hydraulic safety than opposite wood. Plant Cell Environ 26:1365–1371

    Article  Google Scholar 

  • Mayr S, Sperry JS (2010) Freeze–thaw-induced embolism in Pinus contorta: centrifuge experiments validate the ‘thaw-expansion hypothesis’ but conflict with ultrasonic emission data. New Phytol 185:1016–1024

    Article  PubMed  Google Scholar 

  • Mayr S, Schwienbacher F, Bauer H (2003) Winter at the alpine timberline. Why does embolism occur in Norway spruce but not in stone pine? Plant Physiol 131:780–792

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mayr S, Hacke U, Schmid P, Schwienbacher F, Gruber A (2006) Frost drought in conifers at the alpine timberline: xylem dysfunction and adaptations. Ecology 87:3175–3185

    Article  PubMed  Google Scholar 

  • Mayr S, Cochard H, Ameglio T, Kikuta SB (2007) Embolism formation during freezing in the wood of Picea abies. Plant Physiol 143:60–67

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mayr S, Schmid P, Beikircher B (2012) Plant water relations in alpine winter. In: Lutz C (ed) Plants in alpine region: cell physiology of adaptation and survival strategies. Springer, Wien, pp 153–161

    Chapter  Google Scholar 

  • Mayr S, Schmid P, Laur J, Rosner S, Charra-Vaskou K, Damon B et al (2014) Uptake of water via branches helps timberline conifers refill embolized xylem in late winter. Plant Physiol 164:1731–1740

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McCulloh KA, Johnson DM, Meinzer FC, Lachenbruch B (2011) An annual pattern of native embolism in upper branches of four tall conifer species. Am J Bot 98:1007–1015

    Article  PubMed  Google Scholar 

  • Meinzer FC, McCulloh KA (2013) Xylem recovery from drought-induced embolism: where is the hydraulic point of no return? Tree Physiol 33:331–334

    Article  PubMed  Google Scholar 

  • Millard P, Grelet GA (2010) Nitrogen storage and remobilization by trees: ecophysiological relevance in a changing world. Tree Physiol 30:1083–1095

    Article  CAS  PubMed  Google Scholar 

  • Millard P, Hester A, Wendler R, Baillie G (2001) Interspecific defoliation responses of trees depend on sites of winter nitrogen storage. Funct Ecol 15:535–543

    Article  Google Scholar 

  • Morgenstern EK (1996) Geographic variation in forest trees: genetic basis and application of knowledge in silviculture. UBC Press, Vancouver, p 209

    Google Scholar 

  • Nardini A, Lo Gullo MA, Salleo S (2011) Refilling embolized xylem conduits: is it a matter of phloem unloading? Plant Sci 180:604–611

    Article  CAS  PubMed  Google Scholar 

  • Ogasa M, Taneda H, Ooeda H, Ohtsuka A, Maruta E (2019) Repair of severe winter xylem embolism supports summer water transport and carbon gain in a flagged crown of the subalpine conifer Abies veitchii. Tree Physiol (in press)

  • Oleksyn J, Modrzynski J, Tjoelker MG, Zytkowiak R, Reich PB (1998) Growth and physiology of Picea abies populations from elevational transects: common garden evidence for altitudinal ecotypes and cold adaptation. Funct Ecol 12:573–590

    Article  Google Scholar 

  • Olson ME, Anfodillo T, Rosell JA, Petit G, Crivellaro A, Isnard S, Leon-Gomez C, Alvarado-Cardenas LO, Castorena M (2014) Universal hydraulics of the flowering plants: vessel diameter scales with stem length across angiosperm lineages, habits and climates. Ecol Lett 17:988–997

    Article  PubMed  Google Scholar 

  • Petit G, Anfodillo T, Carraro V, Grani F, Carrer M (2011) Hydraulic constraints limit height growth in trees at high altitude. New Phytol 189:241–252

    Article  PubMed  Google Scholar 

  • Pittermann J, Sperry JS (2006) Analysis of freeze–thaw embolism in conifers. The interaction between cavitation pressure and tracheid size. Plant Physiol 140:374–382

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pittermann J, Choat B, Jansen S, Stuart SA, Lynn L, Dawson TE (2010) The relationships between xylem safety and hydraulic efficiency in the Cupressaceae: the evolution of pit membrane form and function. Plant Physiol 153:1919–1931

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rehfeldt GE (1983) Adaptation of Pinus contorta populations to heterogeneous environments in northern Idaho. Can J For Res 13:405–411

    Article  Google Scholar 

  • Reinhardt K, Castanha C, Germino MJ, Kueppers LM (2011) Ecophysiological variation in two provenances of Pinus flexilis seedlings across an elevational gradient from forest to alpine. Tree Physiol 31:615–625

    Article  PubMed  Google Scholar 

  • Sáenz-Romero C, Lamy J, Loya-Rebollar E, Plaza-Aguilar A, Burlett R, Lobit P et al (2013) Genetic variation of drought-induced cavitation resistance among Pinus hartwegii populations from an altitudinal gradient. Acta Physiol Plant 35:2905–2913

    Article  CAS  Google Scholar 

  • Sakai A, Larcher W (1987) Frost survival of plants: responses and adaptation to freezing stress. Springer, Berlin

    Book  Google Scholar 

  • Savage VM, Bentley LP, Enquist BJ, Sperry JS, Smith DD, Reich PB, von Allmen EI (2010) Hydraulic trade-offs and space filling enable better predictions of vascular structure and function in plants. Proc Natl Acad Sci USA 107:22722–22727

    Article  PubMed  PubMed Central  Google Scholar 

  • Scholz FG, Bucci SJ, Goldstein G, Meinzer FC, Franco AC, Miralles-Wilhelm F (2007) Biophysical properties and functional significance of stem water storage tissues in neotropical savanna trees. Plant Cell Environ 30:236–248

    Article  PubMed  Google Scholar 

  • Schweingruber FH, Börner A, Schulze ED (2011) Atlas of stem anatomy in herbs, shrubs and trees. Springer, Berlin

    Book  Google Scholar 

  • Sebastian-Azcona J, Hacke U, Hamann A (2018) Adaptations of white spruce to climate: strong intraspecific differences in cold hardiness linked to survival. Ecol Evol 8:1758–1768

    Article  PubMed  PubMed Central  Google Scholar 

  • Sevanto S (2018) Drought impacts on phloem transport. Curr Opin Plant Biol 43:76–81

    Article  PubMed  Google Scholar 

  • Sevanto S, Holbrook NM, Ball MC (2012) Freeze/thaw-induced embolism: probability of critical bubble formation depends on speed of ice formation. Front Plant Sci 3:107

    Article  PubMed  PubMed Central  Google Scholar 

  • Smith WK, Germino MJ, Hancock TE, Johnson DM (2003) Another perspective on altitudinal limits of alpine timberlines. Tree Physiol 23:1101–1112

    Article  PubMed  Google Scholar 

  • Sparks JP, Campbell GS, Black AR (2001) Water content, hydraulic conductivity, and ice formation in winter stems of Pinus contorta: a TDR case study. Oecologia 127:468–475

    Article  PubMed  Google Scholar 

  • Sperry JS, Nichols KL, Sullivan JEM, Eastlack SE (1994) Xylem embolism in ring-porous, diffuse-porous, and coniferous trees of northern Utah and interior Alaska. Ecology 75:1736–1752

    Article  Google Scholar 

  • Suyama Y, Yoshimatsu H, Tsumura Y (2000) Molecular phylogenetic position of Japanese Abies (Pinaceae) based on chloroplast DNA sequences. Mol Phylogenetics Evol 16:271–277

    Article  CAS  Google Scholar 

  • Taneda H, Tateno M (2005) Hydraulic conductivity, photosynthesis and leaf water balance in six evergreen woody species from fall to winter. Tree Physiol 25:299–306

    Article  PubMed  Google Scholar 

  • Taneda H, Terashima I (2012) Co-ordinated development of the leaf midrib xylem with the lamina in Nicotiana tabacum. Ann Bot 110:35–45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Telewski FW, Jaffe MJ (1986a) Thigmomorphogenesis: anatomical, morphological and mechanical analysis of genetically different sibs of Pinus taeda in response to mechanical perturbation. Physiol Plant 66:219–226

    Article  CAS  PubMed  Google Scholar 

  • Telewski FW, Jaffe MJ (1986b) Thigmomorphogenesis: field and laboratory studies of Abies fraseri in response to wind or mechanical perturbation. Physiol Plant 66:211–218

    Article  CAS  PubMed  Google Scholar 

  • Turunen M, Latola K (2005) UV-B radiation and acclimation in timberline plants. Environ Pollut 137:390–403

    Article  CAS  PubMed  Google Scholar 

  • Tyree MT, Zimmermann HM (2002) Xylem structure and the ascent of sap. Springer, Berlin

    Book  Google Scholar 

  • University Forest in Hokkaido (1977) Meteorological observations at different elevations of Mt. Dairoku, the Tokyo University Forest in Hokkaido: records in the period 1972‒1975 and short discussion on them. Misc Inform Univ Tokyo For 21:22–47 (in Japanese)

    Google Scholar 

  • White TL, Adams WT, Neale DB (2007) Forest genetics. CABI Publishing, Cambridge, p 500

    Book  Google Scholar 

  • Yamazaki T (1995) Pinaceae. In: Iwatsuki K, Yamazaki T, Boufford DE, Ohba H (eds) Flora of Japan. Ι. Pteriodophyta and Gymnospermae. Kodansha, Tokyo, pp 266–277

    Google Scholar 

  • Zhang YJ, 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zwieniecki MA, Stone HA, Leigh A, Boyce K, Holbrook NM (2006) Hydraulic design of pine needles: one-dimensional optimization for single-vein leaves. Plant Cell Environ 29:803–809

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank A. Kurahashi for establishing the provenance trial used in this study. We also thank the associated editor and anonymous reviewer for thoughtful comments, N. Kimura and S. Fukuoka for technical assistance, and K. Yazaki and Y. Sano for evaluation of pit architecture using the FE-SEM. This study was financially supported by the Japan Society for the Promotion of Science (JSPS), KAKENHI Grant numbers 16H02554 and 17H03825.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Haruhiko Taneda.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by L. Kalcsits.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (XLSX 20 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Taneda, H., Funayama-Noguchi, S., Mayr, S. et al. Elevational adaptation of morphological and anatomical traits by Sakhalin fir (Abies sachalinensis). Trees 34, 507–520 (2020). https://doi.org/10.1007/s00468-019-01932-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00468-019-01932-4

Keywords

Navigation