Repeated colonization of alpine habitats by Arabidopsis arenosa viewed through freezing resistance and ice management strategies
Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic
Typ dokumentu časopisecké články
Grantová podpora
P 31027
Austrian Science fund
PubMed
35833328
PubMed Central
PMC9804731
DOI
10.1111/plb.13454
Knihovny.cz E-zdroje
- Klíčová slova
- Adaptation, cold acclimation, freezing resistance, ice nucleation, parallel evolution, polyploidization,
- MeSH
- aklimatizace MeSH
- Arabidopsis * genetika MeSH
- ekosystém MeSH
- fotosystém II - proteinový komplex MeSH
- led MeSH
- rostliny MeSH
- tetraploidie MeSH
- zmrazování MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- fotosystém II - proteinový komplex MeSH
- led MeSH
Success or failure of plants to cope with freezing temperatures can critically influence plant distribution and adaptation to new habitats. Especially in alpine environments, frost is a likely major selective force driving adaptation. In Arabidopsis arenosa (L.) Lawalrée, alpine populations have evolved independently in different mountain ranges, enabling studying mechanisms of acclimation and adaptation to alpine environments. We tested for heritable, parallel differentiation in freezing resistance, cold acclimation potential and ice management strategies using eight alpine and eight foothill populations. Plants from three European mountain ranges (Niedere Tauern, Făgăraș and Tatra Mountains) were grown from seeds of tetraploid populations in four common gardens, together with diploid populations from the Tatra Mountains. Freezing resistance was assessed using controlled freezing treatments and measuring effective quantum yield of photosystem II, and ice management strategies by infrared video thermography and cryomicroscopy. The alpine ecotype had a higher cold acclimation potential than the foothill ecotype, whereby this differentiation was more pronounced in tetraploid than diploid populations. However, no ecotypic differentiation was found in one region (Făgăraș), where the ancient lineage had a different evolutionary history. Upon freezing, an ice lens within a lacuna between the palisade and spongy parenchyma tissues was formed by separation of leaf tissues, a mechanism not previously reported for herbaceous species. The dynamic adjustment of freezing resistance to temperature conditions may be particularly important in alpine environments characterized by large temperature fluctuations. Furthermore, the formation of an extracellular ice lens may be a useful strategy to avoid tissue damage during freezing.
Department of Botany and Biodiversity Research University of Vienna Vienna Austria
Department of Botany Charles University of Prague Prague Czech Republic
Department of Botany University of Innsbruck Innsbruck Austria
Zobrazit více v PubMed
Armstrong J.J., Takebayashi N., Sformo T., Wolf D.E. (2015) Cold tolerance in Arabidopsis kamchatica . American Journal of Botany, 102, 439–448. PubMed
Arnold B., Kim S.‐T., Bomblies K. (2015) Single geographic origin of a widespread autotetraploid Arabidopsis arenosa lineage followed by interploidy admixture. Molecular Biology and Evolution, 32, 1382–1395. PubMed
Berglund A.B.N., Dahlgren S., Westerbergh A. (2004) Evidence for parallel evolution and site‐specific selection of serpentine tolerance in Cerastium alpinum during the colonization of Scandinavia. New Phytologist, 161, 199–209.
Bodner M., Beck E. (1987) Effect of supercooling and freezing on photosynthesis in freezing tolerant leaves of afro‐alpine ‘giant rosette’ plants. Oecologia, 72, 366–371. PubMed
Bohutínská M., Vlček J., Yair S., Laenen B., Konečná V., Fracassetti M., Slotte T., Kolář F. (2021) Genomic basis of parallel adaptation varies with divergence in Arabidopsis and its relatives. Proceedings of the National Academy of Sciences of the United States of America, 118, 2022713118. PubMed PMC
Brochmann C., Borgen L., Stabbetorp O.E. (2000) Multiple diploid hybrid speciation of the Canary Island endemic Argyranthemum sundingii (Asteraceae). Plant Systematics and Evolution, 220, 77–92.
Bucher S.F., Feiler R., Buchner O., Neuner G., Rosbakh S., Leiterer M., Römermann C. (2018) Temporal and spatial trade‐offs between resistance and performance traits in herbaceous plant species. Environmental and Experimental Botany, 157, 187–196.
Buchner O., Neuner G. (2010) Freezing cytorrhysis and critical temperature thresholds for photosystem II in the peat moss Sphagnum capillifolium . Protoplasma, 243, 63–71. PubMed
Burnham K.P., Anderson D.R. (2002) Model selection and multimodel inference: A practical information‐theoretic approach, 2nd edition. Springer, New York, USA.
Clausen J., Keck D.D., Hiesey W.M. (1940) Experimental studies on the nature of species. I. Effect of varied environments on western North American plants. Carnegie Institution of Washington, Washington, DC, USA.
Comai L. (2005) The advantages and disadvantages of being polyploid. Nature Reviews Genetics, 6, 836–846. PubMed
Foster S.A., McKinnon G.E., Steane D.A., Potts B.M., Vaillancourt R.E. (2007) Parallel evolution of dwarf ecotypes in the forest tree Eucalyptus globulus . New Phytologist, 175, 370–380. PubMed
Gianoli E., Inostroza P., Zuniga‐Feest A., Reyes‐Diaz M., Cavieres L.A., Bravo L.A., Corcuera L.J. (2004) Ecotypic differentiation in morphology and cold resistance in populations of Colobanthus quitensis (Caryophyllaceae) from the Andes of Central Chile and the maritime Antarctic. Arctic, Antarctic, and Alpine Research, 36, 484–489.
Gilmour S.J., Hajela R.K., Thomashow M.F. (1988) Cold‐acclimation in Arabidopsis thaliana . Plant Physiology, 87, 745–750. PubMed PMC
Gusta L.V., Wisniewski M. (2013) Understanding plant cold hardiness: an opinion. Physiologia Plantarum, 147, 4–14. PubMed
Hacker J., Neuner G. (2007) Ice propagation in plants visualized at the tissue level by infrared differential thermal analysis (IDTA). Tree Physiology, 27, 1661–1670. PubMed
Hacker J., Neuner G. (2008) Ice propagation in dehardened alpine plant species studied by infrared differential thermal analysis (IDTA). Arctic, Antarctic, and Alpine Research, 40, 660–670.
Hacker J., Ladinig U., Wagner J., Neuner G. (2011) Inflorescences of alpine cushion plants freeze autonomously and may survive subzero temperatures by supercooling. Plant Science, 180, 149–156. PubMed PMC
Han T.S., Zheng Q.J., Onstein R.E., Rojas-Andrés B.M., Hauenschild F., Muellner-Riehl A.N., Xing Y.W. (2020) Polyploidy promotes species diversification of Allium through ecological shifts. New Phytologist, 225, 571–583. PubMed
Hannah M.A., Wiese D., Freund S., Fiehn O., Heyer A.G., Hincha D.K. (2006) Natural genetic variation of freezing tolerance in Arabidopsis . Plant Physiology, 142, 98–112. PubMed PMC
Hoermiller I.I., Ruschhaupt M., Heyer A.G. (2018) Mechanisms of frost resistance in Arabidopsis thaliana . Planta, 248, 827–835. PubMed
Klotke J., Kopka J., Gatzke N., Heyer A.G. (2004) Impact of soluble sugar concentrations on the acquisition of freezing tolerance in accessions of Arabidopsis thaliana with contrasting cold adaptation – Evidence for a role of raffinose in cold acclimation. Plant, Cell & Environment, 27, 1395–1404.
Knight M.R., Knight H. (2012) Low‐temperature perception leading to gene expression and cold tolerance in higher plants. New Phytologist, 195, 737–751. PubMed
Knotek A., Konečná V., Wos G., Požárová D., Šrámková G., Bohutínská M., Zeisek V., Marhold K., Kolář F. (2020) Parallel alpine differentiation in Arabidopsis arenosa . Frontiers in Plant Science, 11, 561526. PubMed PMC
Kolář F., Fuxová G., Záveská E., Nagano A.J., Hyklová L., Lučanová M., Kudoh H., Marhold K. (2016a) Northern glacial refugia and altitudinal niche divergence shape genome‐wide differentiation in the emerging plant model Arabidopsis arenosa . Molecular Ecology, 25, 3929–3949. PubMed
Kolář F., Lucanova M., Zaveska E., Fuxova G., Mandakova T., Spaniel S., Senko D., Svitok M., Kolnik M., Gudzinskas Z., Marhold K. (2016b) Ecological segregation does not drive the intricate parapatric distribution of diploid and tetraploid cytotypes of the Arabidopsis arenosa group (Brassicaceae). Biological Journal of the Linnean Society, 119, 673–688.
Körner C. (2003) Alpine plant life: functional plant ecology of High Mountain ecosystems, 2nd edition. Springer, Berlin, Germany.
Kuprian E., Briceño V.F., Wagner J., Neuner G. (2014) Ice barriers promote supercooling and prevent frost injury in reproductive buds, flowers and fruits of alpine dwarf shrubs throughout the summer. Environmental and Experimental Botany, 106, 4–12. PubMed PMC
Kuprian E., Munkler C., Resnyak A., Zimmermann S., Tuong T.D., Gierlinger N., Müller T., Livingston D.P., Neuner G. (2017) Complex bud architecture and cell‐specific chemical patterns enable supercooling of Picea abies bud primordia. Plant, Cell & Environment, 40, 3101–3112. PubMed PMC
Kuznetsova A., Brockhoff P.B., Christensen R.H. (2017) lmerTest package: Tests in linear mixed effects models. Journal of Statistical Software, 82, 1–26.
Ladinig U., Hacker J., Neuner G., Wagner J. (2013) How endangered is sexual reproduction of high‐mountain plants by summer frosts? Frost resistance, frequency of frost events and risk assessment. Oecologia, 171, 743–760. PubMed PMC
Le M.Q., Engelsberger W.R., Hincha D.K. (2008) Natural genetic variation in acclimation capacity at sub‐zero temperatures after cold acclimation at 4 °C in different Arabidopsis thaliana accessions. Cryobiology, 57, 104–112. PubMed
Li C., Wu N., Liu S. (2005) Development of freezing tolerance in different altitudinal ecotypes of Salix paraplesia . Biologia Plantarum, 49, 65–71.
Liu B., Xia Y.‐P., Krebs S.L., Medeiros J., Arora R. (2019) Seasonal responses to cold and light stresses by two elevational ecotypes of Rhododendron catawbiense: a comparative study of overwintering strategies. Environmental and Experimental Botany, 163, 86–96.
Lomas J., Schlesinger E., Israeli A. (1971) Leaf temperature measurement techniques. Boundary‐Layer Meteorology, 1, 458–465.
Lowry D.B. (2012) Ecotypes and the controversy over stages in the formation of new species. Biological Journal of the Linnean Society, 106, 241–257.
McCully M.E., Canny M., Huang C. (2004) The management of extracellular ice by petioles of frost‐resistant herbaceous plants. Annals of Botany, 94, 665–674. PubMed PMC
Melcher P., Cordell S., Jones T., Scowcroft P., Niemczura W., Giambelluca T., Goldstein G. (2000) Supercooling capacity increases from sea level to tree line in the Hawaiian tree species Metrosideros polymorpha . International Journal of Plant Sciences, 161, 369–379. PubMed
Měsíček J., Goliašová K. (2002) Cardaminopsis (C. A. Mey.) Hayek. In: Goliašová K., Šípošová H. (Eds), Flóra Slovenska. Slovakia, Veda, Bratislava, pp 388–415.
Molina‐Henao Y.F., Hopkins R. (2019) Autopolyploid lineage shows climatic niche expansion but not divergence in Arabidopsis arenosa . American Journal of Botany, 106, 61–70. PubMed
Monnahan P., Kolář F., Baduel P., Sailer C., Koch J., Horvath R., Laenen B., Schmickl R., Paajanen P., Šrámková G., Bohutínská M., Arnold B., Weisman C.M., Marhold K., Slotte T., Bomblies K., Yant L. (2019) Pervasive population genomic consequences of genome duplication in Arabidopsis arenosa . Nature Ecology and Evolution, 3, 457–468. PubMed
Morgan E.J., Čertner M., Lučanová M., Kubíková K., Marhold K., Kolář F. (2020) Niche similarity in diploid‐autotetraploid contact zones of Arabidopsis arenosa across spatial scales. American Journal of Botany, 107, 1375–1388. PubMed
Neuner G. (2014) Frost resistance in alpine woody plants. Frontiers in Plant Science, 5, 654. PubMed PMC
Neuner G., Buchner O. (1999) Assessment of foliar frost damage: a comparison of in vivo chlorophyll fluorescence with other viability tests. Angewandte Botanik, 73, 50–54.
Neuner G., Hacker J. (2012) Ice formation and propagation in alpine plants, Plants in Alpine Regions. Springer, Vienna, Austria, pp 163–174.
Neuner G., Lichtenberger E. (2020) Infrared thermal analysis of plant freezing processes. In: Hincha D.K., Zuther E. (Eds), Plant cold acclimation. Springer, Cham, Switzerland, pp 33–41. PubMed
Neuner G., Huber B., Plangger A., Pohlin J.‐M., Walde J. (2020) Low temperatures at higher elevations require plants to exhibit increased freezing resistance throughout the summer months. Environmental and Experimental Botany, 169, 103882.
Novikova P.Y., Brennan I.G., Booker W., Mahony M., Doughty P., Lemmon A.R., Lemmon E.M., Roberts J.D., Yant L., Van de Peer Y., Keogh J.S., Donnellan S.C. (2020) Polyploidy breaks speciation barriers in Australian burrowing frogs Neobatrachus . PLoS Genetics, 16, e1008769. PubMed PMC
Pagter M., Arora R. (2013) Winter survival and deacclimation of perennials under warming climate: Physiological perspectives. Physiologia Plantarum, 147, 75–87. PubMed
Pfennig D.W., Wund M.A., Snell‐Rood E.C., Cruickshank T., Schlichting C.D., Moczek A.P. (2010) Phenotypic plasticity's impacts on diversification and speciation. Trends in Ecology & Evolution, 25, 459–467. PubMed
Preston J.C., Sandve S.R. (2013) Adaptation to seasonality and the winter freeze. Frontiers in Plant Science, 4, 167. PubMed PMC
Rahman T., Shao M., Pahari S., Venglat P., Soolanayakanahally R., Qiu X., Rahman A., Tanino K. (2021) Dissecting the roles of cuticular wax in plant resistance to shoot dehydration and low‐temperature stress in Arabidopsis . International Journal of Molecular Sciences, 22, 1554. PubMed PMC
R Core Team . (2021) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available from https://www.R-project.org/ (accessed 29 April 2022).
Roda F., Ambrose L., Walter G.M., Liu H.L., Schaul A., Lowe A., Pelser P.B., Prentis P., Rieseberg L.H., Ortiz‐Barrientos D. (2013) Genomic evidence for the parallel evolution of coastal forms in the Senecio lautus complex. Molecular Ecology, 22, 2941–2952. PubMed
Sakai A., Larcher W. (1987) Low temperature and frost as environmental factors. In: Sakai A., Larcher W. (Eds), Frost survival of plants. Springer, Berlin, Germany, pp 1–20.
Schat H., Vooijs R., Kuiper E. (1996) Identical major gene loci for heavy metal tolerances that have independently evolved in different local populations and subspecies of Silene vulgaris . Evolution, 50, 1888–1895. PubMed
Schluter D., Clifford E.A., Nemethy M., McKinnon J.S. (2004) Parallel evolution and inheritance of quantitative traits. The American Naturalist, 163, 809–822. PubMed
Schott R.T., Neinhuis C., Roth‐Nebelsick A. (2020) Extracellular ice formation in special intercellular air spaces in Stachys byzantina C. Koch. Feddes Repertorium, 131, 233–243.
Schrieber K., Caceres Y., Engelmann A., Marcora P., Renison D., Hensen I., Muller C. (2020) Elevational differentiation in metabolic cold stress responses of an endemic mountain tree. Environmental and Experimental Botany, 171, 103918.
Soltis P.S., Soltis D.E. (2016) Ancient WGD events as drivers of key innovations in angiosperms. Current Opinion in Plant Biology, 30, 159–165. PubMed
Stearns S.C., Hoekstra R.F. (2005) Evolution, an introduction, 2nd edition. Oxford University Press, Oxford, UK.
Stegner M., Lackner B., Schäfernolte T., Buchner O., Xiao N., Gierlinger N., Holzinger A., Neuner G. (2020a) Winter nights during summer time: Stress physiological response to ice and the facilitation of freezing cytorrhysis by elastic cell wall components in the leaves of a nival species. International Journal of Molecular Sciences, 21, 7042. PubMed PMC
Stegner M., Wagner J., Neuner G. (2020b) Ice accommodation in plant tissues pinpointed by cryo‐microscopy in polarised light. Plant Methods, 16, 1–9. PubMed PMC
Takahashi D., Zuther E., Hincha D.K. (2020) Analysis of changes in plant cell wall composition and structure during cold acclimation. In: Hincha D., Zuther E. (Eds), Plant cold acclimation. Methods in Molecular Biology. Humana, New York, USA. PubMed
Taschler D., Neuner G. (2004) Summer frost resistance and freezing patterns measured in situ in leaves of major alpine plant growth forms in relation to their upper distribution boundary. Plant, Cell & Environment, 27, 737–746.
Thomashow M.F. (1999) Plant cold acclimation: Freezing tolerance genes and regulatory mechanisms. Annual Review of Plant Biology, 50, 571–599. PubMed
Thompson K.A., Osmond M.M., Schluter D. (2019) Parallel genetic evolution and speciation from standing variation. Evolution Letters, 3, 129–141. PubMed PMC
Trucchi E., Frajman B., Haverkamp T.H., Schönswetter P., Paun O. (2017) Genomic analyses suggest parallel ecological divergence in Heliosperma pusillum (Caryophyllaceae). New Phytologist, 216, 267–278. PubMed PMC
Turesson G. (1922) The species and the variety as ecological units. Hereditas, 3, 100–113.
Uemura M., Joseph R.A., Steponkus P.L. (1995) Cold acclimation of Arabidopsis thaliana (effect on plasma membrane lipid composition and freeze‐induced lesions) . Plant Physiology, 109, 15–30. PubMed PMC
Van de Peer Y., Ashman T.L., Soltis P.S., Soltis D.E. (2021) Polyploidy: an evolutionary and ecological force in stressful times. The Plant Cell, 33, 11–26. PubMed PMC
Vyse K., Pagter M., Zuther E., Hincha D.K. (2019) Deacclimation after cold acclimation – a crucial, but widely neglected part of plant winter survival. Journal of Experimental Botany, 70, 4595–4604. PubMed PMC
Walton W.H. (1982) Instruments for measuring biological microclimates for terrestrial habitats in polar and high alpine regions: a review. Arctic and Alpine Research, 14, 275–286.
Wisniewski M., Gusta L., Neuner G. (2014) Adaptive mechanisms of freeze avoidance in plants: a brief update. Environmental and Experimental Botany, 99, 133–140.
Wos G., Mořkovská J., Bohutínská M., Šrámková G., Knotek A., Lučanová M., Španiel S., Marhold K., Kolář F. (2019) Role of ploidy in colonization of alpine habitats in natural populations of Arabidopsis arenosa . Annals of Botany, 124, 255–268. PubMed PMC
Wos G., Bohutínská M., Nosková J., Mandáková T., Kolář F. (2021) Parallelism in gene expression between foothill and alpine ecotypes in Arabidopsis arenosa . The Plant Journal, 105, 1211–1224. PubMed
Wos G., Arc E., Hülber K., Konečná V., Knotek A., Požárová D., Bertel C., Kaplenig D., Mandáková T., Neuner G., Schönswetter P., Kranner I., Kolář F. (2022) Parallel local adaptation to an alpine environment in Arabidopsis arenosa . Journal of Ecology, in press. 10.1111/1365-2745.13961 DOI
Xin Z., Browse J. (2000) Cold comfort farm: the acclimation of plants to freezing temperatures. Plant, Cell & Environment, 23, 893–902.
Yant L., Hollister J.D., Wright K.M., Arnold B.J., Higgins J.D., Franklin F.C.H., Bomblies K. (2013) Meiotic adaptation to genome duplication in Arabidopsis arenosa . Current Biology, 23, 2151–2156. PubMed PMC
Zuther E., Schulz E., Childs L.H., Hincha D.K. (2012) Clinal variation in the non‐acclimated and cold‐acclimated freezing tolerance of Arabidopsis thaliana accessions. Plant, Cell & Environment, 35, 1860–1878. PubMed
Zuther E., Juszczak I., Lee Y.P., Baier M., Hincha D.K. (2015) Time‐dependent de‐acclimation after cold acclimation in Arabidopsis thaliana accessions. Scientific Reports, 5, 12199. PubMed PMC