Highest Occurring Vascular Plants from Ladakh Provide Wood Anatomical Evidence for a Thermal Limitation of Cell Wall Lignification

. 2025 Feb ; 48 (2) : 1445-1451. [epub] 20241024

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid39449249

Grantová podpora
This research was supported by Czech Science Foundation (# 24-11954S # 23-08049S), ERC Advanced Grant (# 882727) and the ERC Synergy Grant (# 101118880).

As an evolutionary achievement of almost all terrestrial plants, lignin biosynthesis is essential for various mechanical and physiological processes. Possible effects of plant cell wall lignification on large-scale vegetation distribution are, however, not yet fully understood. Here, we present double-stained, wood anatomical stem measurements of 207 perennial herbs (Potentilla pamirica Wolf), which were collected between 5550 and 5850 m asl on the north-western Tibetan Plateau in Ladakh, India. We also measured changes in situ root zone and surface air temperatures along the sampling gradient and applied piecewise structural equation models to assess direct and indirect relationships between the age and size of plants, the degree of cell wall lignification in their stems, and the elevation at which they were growing. Based on the world's highest-occurring vascular plants, the Pamir Cinquefoils, we demonstrate that the amount of lignin in the secondary cell walls decreases significantly with increasing elevation (r = -0.73; p < 0.01). Since elevation is a proxy for temperature, our findings suggest a thermal constrain on lignin biosynthesis at the cold range limit of woody plant growth.

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Abatzoglou, J. T. , Dobrowski S. Z., Parks S. A., and Hegewisch K. C.. 2018. “Terraclimate, a High‐Resolution Global Dataset of Monthly Climate and Climatic Water Balance from 1958–2015.” Scientific Data 5: 170191. PubMed PMC

Allee, W. C. 1931. Animal Aggregations. Chicago: University of Chicago Press.

Angel, R. , Conrad R., Dvorsky M., et al. 2016. “The Root‐Associated Microbial Community of the World's Highest Growing Vascular Plants.” Microbial Ecology 72: 394–406. PubMed PMC

Baldacci‐Cresp, F. , Spriet C., Twyffels L., et al. 2020. “A Rapid and Quantitative Safranin‐Based Fluorescent Microscopy Method to Evaluate Cell Wall Lignification.” The Plant Journal 102: 1074–1089. PubMed

Barros, J. , Serk H., Granlund I., and Pesquet E.. 2015. “The Cell Biology of Lignification in Higher Plants.” Annals of Botany 115: 1053–1074. PubMed PMC

Begum, S. , Nakaba S., Yamagishi Y., Oribe Y., and Funada R.. 2013. “Regulation of Cambial Activity in Relation to Environmental Conditions: Understanding the Role of Temperature in Wood Formation of Trees.” Physiologia Plantarum 147: 46–54. PubMed

Bond, J. , Donaldson L., Hill S., and Hitchcock K.. 2008. “Safranine Fluorescent Staining of Wood Cell Walls.” Biotechnic & Histochemistry 83: 161–171. PubMed

Büntgen, U. 2023. “Experimental Evidence for a Thermal Limitation of Plant Cell Wall Lignification at the Alpine Treeline.” Alpine Botany 133: 179–182.

Büntgen, U. , Crivellaro A., Arseneault D., et al. 2022. “Global Wood Anatomical Perspective on the Onset of the Late Antique Little Ice Age (LALIA) in the mid‐6th Century Ce.” Science Bulletin 67: 2336–2344. PubMed

Büntgen, U. , Hellmann L., Tegel W., et al. 2015. “Temperature‐Induced Recruitment Pulses of Arctic Dwarf Shrub Communities.” Journal of Ecology 103: 489–501.

Büntgen, U. , Palosse A., Dolezal J., and Liebhold A.. 2024. “Introducing the Concepts of Range‐Pinning and Allee Effects to Explain Reduced Temperature Sensitivity of Global Treeline Dynamics.” Global Change Biology 30: e17288. PubMed

Büntgen, U. , Piermattei A., Dolezal J., Dupree P., and Crivellaro A.. 2023. “Reply To: Biogeographic Implications of Plant Stature and Microclimate in Cold Regions.” Communications Biology 6: 662. PubMed PMC

Chlumská, Z. , Liancourt P., Hartmann H., et al. 2022. “Species‐ and Compound‐Specific Dynamics of Nonstructural Carbohydrates Toward the World's Upper Distribution of Vascular Plants.” Environmental and Experimental Botany 201: 104985.

Courchamp, F. , Berec L., and Gascoigne J.. 2008. Allee Effects in Ecology and Conservation. Oxford: Oxford Academic.

Crivellaro, A. , and Büntgen U.. 2020. “New Evidence of Thermally‐Constraint Plant Cell Wall Lignification.” Trends in Plant Science 24: 322–324. PubMed

Crivellaro, A. , Piermattei A., Dolezal J., Dupree P., and Büntgen U.. 2022. “Biogeographic Implication of Temperature‐Induced Plant Cell Wall Lignification.” Communications Biology 5: 767. PubMed PMC

Dolezal, J. , Dvorsky M., Kopecky M., et al. 2016. “Vegetation Dynamics at the Upper Elevational Limit of Vascular Plants in Himalaya.” Scientific Reports 6: 24881. PubMed PMC

Dolezal, J. , Jandova V., Macek M., et al. 2021a. “Climate Warming Drives Himalayan Alpine Plant Growth and Recruitment Dynamics.” Journal of Ecology 109: 179–190.

Dolezal, J. , Jandova V., Macek M., and Liancourt P.. 2021b. “Contrasting Biomass Allocation Responses Across Ontogeny and Stress Gradients Reveal Plant Adaptations to Drought and Cold.” Functional Ecology 35: 32–42.

Dvorský, M. , Doležal J., de Bello F., Klimešová J., and Klimeš L.. 2011. “Vegetation Types of East Ladakh: Species and Growth Form Composition Along Main Environmental Gradients.” Applied Vegetation Science 14: 132–147.

Esper, J. , Torbenson M., and Büntgen U.. 2024. “2023 Summer Warmth Unparalleled over the Past 2,000 Years.” Nature 631: 94–97. PubMed

Gärtner, H. , Cherubini P., Fonti P., et al. 2015. “Technical Challenges in Tree‐Ring Research Including Wood Anatomy and Dendroecology.” Journal of Visualized Experiments 97: e52337. PubMed PMC

Greaves, C. , Crivellaro A., Piermattei A., et al. 2023. “Remarkably High Blue Ring Occurrence in Estonian Scots Pines in 1976 Reveals Wood Anatomical Evidence of Extreme Autumnal Cooling.” Trees 37: 511–522.

Hao, Z. , and Mohnen D.. 2014. “A Review of Xylan and Lignin Biosynthesis: Foundation for Studying Arabidopsis Irregular Xylem Mutants with Pleiotropic Phenotypes.” Critical Reviews in Biochemistry and Molecular Biology 49: 212–241. PubMed

von Humboldt, A. , and Bonpland A.. 1805. Essai sur la Géographie des Plantes. Chez Levrault. Libraires: Schoell et Compagnie.

Körner, C. 2012. Alpine Treelines. Basel: Springer.

Körner, C. , Fajardo A., and Hiltbrunner E.. 2023. “Biogeographic Implications of Plant Stature and Microclimate in Cold Regions.” Communications Biology 6, 663. PubMed PMC

Körner, C. , Lenz A., and Hoch G.. 2023. “Chronic in Situ Tissue Cooling Does Not Reduce Lignification at the Swiss Treeline but Enhances the Risk of ‘Blue’ Frost Rings.” Alpine Botany 133, 63–67. PubMed PMC

Kumar, M. , Campbell L., and Turner S.. 2016. “Secondary Cell Walls: Biosynthesis and Manipulation.” Journal of Experimental Botany 67: 515–531. PubMed

Lefcheck, J. S. 2016. “Piecewisesem: Piecewise Structural Equation Modelling in R for Ecology, Evolution, and Systematics.” Methods in Ecology and Evolution 7: 573–579.

Liu, Q. , Luo L., and Zheng L.. 2018. “Lignins: Biosynthesis and Biological Functions in Plants.” International Journal of Molecular Sciences 19: 335. PubMed PMC

Meents, M. J. , Watanabe Y., and Samuels A. L.. 2018. “The Cell Biology of Secondary Cell Wall Biosynthesis.” Annals of Botany 121: 1107–1125. PubMed PMC

Mellerowicz, E. J. , Baucher M., Sundberg B., and Boerjan W.. 2001. “Unravelling Cell Wall Formation in the Woody Dicot Stem.” Plant Molecular Biology 47: 239–274. PubMed

De Micco, V. , and Aronne G.. 2007. “Combined Histochemistry and Autofluorescence for Identifying Lignin Distribution in Cell Walls.” Biotechnic & Histochemistry 82: 209–216. PubMed

Moura, J. C. M. S. , Bonine C. A. V., De Oliveira Fernandes Viana J., Dornelas M. C., and Mazzafera P.. 2010. “Abiotic and Biotic Stresses and Changes in the Lignin Content and Composition in Plants.” Journal of Integrative Plant Biology 52: 360–376. PubMed

Niklas, K. J. , Cobb E. D., and Matas A. J.. 2017. “The Evolution of Hydrophobic Cell Wall Biopolymers: from Algae to Angiosperms.” Journal of Experimental Botany 68: 5261–5269. PubMed

Palosse, A. , Piermattei A., Esper J., et al. 2024. “Temperature‐Induced Germination Pulses above the Alpine Tree Line.” Arctic, Antarctic, and Alpine Research 56: 2362447.

Piermattei, A. , Crivellaro A., Carrer M., and Urbinati C.. 2015. “The “Blue Ring”: Anatomy and Formation Hypothesis of a New Tree‐Ring Anomaly in Conifers.” Trees 29: 613–620.

Piermattei, A. , Crivellaro A., Krusic P. J., et al. 2020. “A Millennium‐Long ‘Blue Ring’ Chronology from the Spanish Pyrenees Reveals Severe Ephemeral Summer Cooling after Volcanic Eruptions.” Environmental Research Letters 15: 124016.

Piquemal, J. , Lapierre C., Myton K., et al. 1998. “Down Regulation of Cinnamoyl Coa Reductase Induces Significant Changes of Lignin Profiles in Transgenic Tobacco Plants.” The Plant Journal 13: 71–83.

Plomion, C. , Leprovost G., and Stokes A.. 2001. “Wood Formation in Trees.” Plant Physiology 127: 1513–1523. PubMed PMC

Polo, C. C. , Pereira L., Mazzafera P., et al. 2020. “Correlations between Lignin Content and Structural Robustness in Plants Revealed By X‐Ray Ptychography.” Scientific Reports 10: 6023. PubMed PMC

Řeháková, K. , Capkova K., Hrouzek P., Kolizek M., and Dolezal J.. 2017. “Microbial Photosynthetic and Photoprotective Pigments in Himalayan Soils Originating from Different Elevations and Successional Stages.” Soil Biology & Biochemistry 132: 153–164.

Renault, H. , Werck‐Reichhart D., and Weng J.‐K.. 2019. “Harnessing Lignin Evolution for Biotechnological Applications.” Current Opinion in Biotechnology 56: 105–111. PubMed

Rossi, S. , Deslauriers A., Anfodillo T., and Carraro V.. 2007. “Evidence of Threshold Temperatures for Xylogenesis in Conifers at High Altitudes.” Oecologia 152: 1–12. PubMed

Schenk, H. J. , Espino S., Rich‐Cavazos S. M., and Jansen S.. 2018. “From the Sap's Perspective: The Nature of Vessel Surfaces in Angiosperm Xylem.” American Journal of Botany 105: 172–185. PubMed

Srebotnik, E. , and Messner K.. 1994. “A Simple Method That Uses Differential Staining and Light Microscopy to Assess the Selectivity of Wood Delignification by White Rot Fungi.” Applied and Environmental Microbiology 60: 1383–1386. PubMed PMC

Tomczyk, M. , and Latté K. P.. 2009. “Potentilla—A Review of Its Phytochemical and Pharmacological Profile.” Journal of Ethnopharmacology 122: 184–204. PubMed

Vazquez‐Cooz, I. , and Meyer R. W.. 2002. “A Differential Staining Method to Identify Lignified and Unlignified Tissues.” Biotechnic & Histochemistry 77: 277–282. PubMed

Weng, J.‐K. , and Chapple C.. 2010. “The Origin and Evolution of Lignin Biosynthesis.” New Phytologist 187: 273–285. PubMed

Zhong, R. , and Ye Z.‐H.. 2009. “Transcriptional Regulation of Lignin Biosynthesis.” Plant Signaling & Behavior 4: 1028–1034. PubMed PMC

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