Pollen thermotolerance of a widespread plant, Lotus corniculatus, in response to climate warming: possible local adaptation of populations from different elevations
Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
38708360
PubMed Central
PMC11067902
DOI
10.7717/peerj.17148
PII: 17148
Knihovny.cz E-zdroje
- Klíčová slova
- Elevational gradient, Heat stress, Local adaptation, Plant reproduction, Pollen, Pollen viability, Pollination, Thermotolerance,
- MeSH
- aklimatizace fyziologie MeSH
- fyziologická adaptace fyziologie MeSH
- globální oteplování MeSH
- klíčení fyziologie MeSH
- klimatické změny MeSH
- Lotus * fyziologie růst a vývoj MeSH
- nadmořská výška MeSH
- pyl * fyziologie MeSH
- teplota MeSH
- termotolerance * fyziologie MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
One of the most vulnerable phases in the plant life cycle is sexual reproduction, which depends on effective pollen transfer, but also on the thermotolerance of pollen grains. Pollen thermotolerance is temperature-dependent and may be reduced by increasing temperature associated with global warming. A growing body of research has focused on the effect of increased temperature on pollen thermotolerance in crops to understand the possible impact of temperature extremes on yield. Yet, little is known about the effects of temperature on pollen thermotolerance of wild plant species. To fill this gap, we selected Lotus corniculatus s.l. (Fabaceae), a species common to many European habitats and conducted laboratory experiments to test its pollen thermotolerance in response to artificial increase in temperature. To test for possible local adaptation of pollen thermal tolerance, we compared data from six lowland (389-451 m a.s.l.) and six highland (841-1,030 m a.s.l.) populations. We observed pollen germination in vitro at 15 °C, 25 °C, 30 °C, and 40 °C. While lowland plants maintained a stable germination percentage across a broad temperature range (15-30 °C) and exhibited reduced germination only at extremely high temperatures (40 °C), highland plants experienced reduced germination even at 30 °C-temperatures commonly exceeded in lowlands during warm summers. This suggests that lowland populations of L. corniculatus may be locally adapted to higher temperature for pollen germination. On the other hand, pollen tube length decreased with increasing temperature in a similar way in lowland and highland plants. The overall average pollen germination percentage significantly differed between lowland and highland populations, with highland populations displaying higher germination percentage. On the other hand, the average pollen tube length was slightly smaller in highland populations. In conclusion, we found that pollen thermotolerance of L. corniculatus is reduced at high temperature and that the germination of pollen from plant populations growing at higher elevations is more sensitive to increased temperature, which suggests possible local adaptation of pollen thermotolerance.
Department of Biotechnology and Biosciences University of Milano Bicocca Milan Italy
Department of Zoology Faculty of Science University of South Bohemia České Budějovice Czech Republic
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Acar I, Kakani VG. The effects of temperature on in vitro pollen germination and pollen tube growth of Pistacia spp. Scientia Horticulturae. 2010;125(4):569–572. doi: 10.1016/j.scienta.2010.04.040. DOI
Aitken SN, Yeaman S, Holliday JA, Wang T, Curtis-McLane S. Adaptation, migration or extirpation: climate change outcomes for tree populations. Evolutionary Applications. 2008;1(1):95–111. doi: 10.1111/j.1752-4571.2007.00013.x. PubMed DOI PMC
Akter A, Klečka J. Water stress and nitrogen supply affect floral traits and pollination of the white mustard, Sinapis alba (Brassicaceae) PeerJ. 2022;10(11):e13009. doi: 10.7717/peerj.13009. PubMed DOI PMC
Alberto FJ, Aitken SN, Alía R, González-Martínez SC, Hänninen H, Kremer A, Lefèvre F, Lenormand T, Yeaman S, Whetten R, Savolainen O. Potential for evolutionary responses to climate change–evidence from tree populations. Global Change Biology. 2013;19(6):1645–1661. doi: 10.1111/gcb.12181. PubMed DOI PMC
Aronne G. Effects of relative humidity and temperature stress on pollen viability of Cistus incanus and Myrtus communis. Grana. 1999;38(6):364–367. doi: 10.1080/00173130050136154. DOI
Bates D, Mächler M, Bolker B, Walker S. Fitting linear mixed-effects models using lme4. Journal of Statistical Software. 2015;67(1):1–48. doi: 10.18637/jss.v067.i01. DOI
Bheemanahalli R, Ramamoorthy P, Poudel S, Samiappan S, Wijewardane N, Reddy KR. Effects of drought and heat stresses during reproductive stage on pollen germination, yield, and leaf reflectance properties in maize (Zea mays L.) Plant Direct. 2022;6(8):2825. doi: 10.1002/pld3.434. PubMed DOI PMC
Bheemanahalli R, Sunoj VSJ, Saripalli G, Prasad PVV, Balyan HS, Gupta PK, Grant N, Gill KS, Jagadish SVK. Quantifying the impact of heat stress on pollen germination, seed set, and grain filling in spring wheat. Crop Science. 2019;59(2):684–696. doi: 10.2135/cropsci2018.05.0292. DOI
Biella P, Bogliani G, Cornalba M, Manino A, Neumayer J, Porporato M, Rasmont P, Milanesi P. Distribution patterns of the cold adapted bumblebee Bombus alpinus in the Alps and hints of an uphill shift (Insecta: Hymenoptera: Apidae) Journal of Insect Conservation. 2017;21(2):357–366. doi: 10.1007/s10841-017-9983-1. DOI
Brewbaker JL, Kwack BH. The essential role of calcium ion in pollen germination and pollen tube growth. American Journal of Botany. 1963;50(9):859–865. doi: 10.1002/j.1537-2197.1963.tb06564.x. DOI
Brink RA. The physiology of pollen I. The requirements for growth. American Journal of Botany. 1924;11(4):218–228. doi: 10.1002/j.1537-2197.1924.tb05773.x. DOI
Chytrý M. Physical geography of the Czech Republic. In: Chytrý M, Danihelka J, Kaplan Z, Pyšek P, editors. Flora and Vegetation of the Czech Republic. Plant and Vegetation. Cham: Springer International Publishing; 2017. pp. 1–23.
Chytrý M, Danihelka J, Kaplan Z, Wild J, Holubová D, Novotný P, Řezníčková M, Rohn M, Dřevojan P, Grulich V, Klimešová J, Lepš J, Lososová Z, Pergl J, Sádlo J, Šmarda P, Štěpánková P, Tichý L, Axmanová I, Bartušková A, Blažek P, Chrtek J, Fischer FM, Guo W-Y, Herben T, Janovský Z, Konečná M, Kühn I, Moravcová L, Petřík P, Pierce S, Prach K, Prokešová H, Štech M, Těšitel J, Těšitelová T, Večeřa M, Zelený D, Pyšek P. Pladias database of the Czech flora and vegetation. Preslia. 2021;93(1):1–87. doi: 10.23855/preslia.2021.001. DOI
Corbet SA. Pollination and the weather. Israel Journal of Botany. 1990;39(1–2):13–30. doi: 10.1080/0021213X.1990.10677131. DOI
Das S, Krishnan P, Nayak M, Ramakrishnan B. High temperature stress effects on pollens of rice (Oryza sativa L.) genotypes. Environmental and Experimental Botany. 2014;101(3):36–46. doi: 10.1016/j.envexpbot.2014.01.004. DOI
Descamps C, Quinet M, Baijot A, Jacquemart A-L. Temperature and water stress affect plant-pollinator interactions in Borago officinalis (Boraginaceae) Ecology and Evolution. 2018;8(6):3443–3456. doi: 10.1002/ece3.3914. PubMed DOI PMC
Du G, Xu J, Gao C, Lu J, Li Q, Du J, Lv M, Sun X. Effect of low storage temperature on pollen viability of fifteen herbaceous peonies. Biotechnology Reports. 2019;21(6):e00309. doi: 10.1016/j.btre.2019.e00309. PubMed DOI PMC
Eckert CG, Kalisz S, Geber MA, Sargent R, Elle E, Cheptou P-O, Goodwillie C, Johnston MO, Kelly JK, Moeller DA, Porcher E, Ree RH, Vallejo-Marín M, Winn AA. Plant mating systems in a changing world. Trends in Ecology & Evolution. 2010;25(1):35–43. doi: 10.1016/j.tree.2009.06.013. PubMed DOI
Fazlioglu F, Wan JSH, Chen L. Latitudinal shifts in mangrove species worldwide: evidence from historical occurrence records. Hydrobiologia. 2020;847(19):4111–4123. doi: 10.1007/s10750-020-04403-x. DOI
Fick SE, Hijmans RJ. WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. International Journal of Climatology. 2017;37(12):4302–4315. doi: 10.1002/joc.5086. DOI
Firon N, Pressman E, Meir S, Khoury R, Altahan L. Ethylene is involved in maintaining tomato (Solanum lycopersicum) pollen quality under heat-stress conditions. AOB PLANTS. 2012;2012:pls024. doi: 10.1093/aobpla/pls024. PubMed DOI PMC
Flores-Rentería L, Whipple AV, Benally GJ, Patterson A, Canyon B, Gehring CA. Higher temperature at lower elevation sites fails to promote acclimation or adaptation to heat stress during pollen germination. Frontiers in Plant Science. 2018;9:536. doi: 10.3389/fpls.2018.00536. PubMed DOI PMC
Freeman BG, Lee-Yaw JA, Sunday JM, Hargreaves AL. Expanding, shifting and shrinking: the impact of global warming on species’ elevational distributions. Global Ecology and Biogeography. 2018;27(11):1268–1276. doi: 10.1111/geb.12774. DOI
He G, Hu F, Ming J, Liu C, Yuan S. Pollen viability and stigma receptivity in Lilium during anthesis. Euphytica. 2017;213(10):231. doi: 10.1007/s10681-017-2019-9. DOI
Hebbar KB, Rose HM, Nair AR, Kannan S, Niral V, Arivalagan M, Gupta A, Samsudeen K, Chandran KP, Chowdappa P, Vara Prasad PV. Differences in in vitro pollen germination and pollen tube growth of coconut (Cocos nucifera L.) cultivars in response to high temperature stress. Environmental and Experimental Botany. 2018;153(1):35–44. doi: 10.1016/j.envexpbot.2018.04.014. DOI
Hedhly A, Hormaza JI, Herrero M. The effect of temperature on pollen germination, pollen tube growth, and stigmatic receptivity in peach. Plant Biology. 2005;7(5):476–483. doi: 10.1055/s-2005-865850. PubMed DOI
Hedhly A, Hormaza JI, Herrero M. Global warming and sexual plant reproduction. Trends in Plant Science. 2009;14(1):30–36. doi: 10.1016/j.tplants.2008.11.001. PubMed DOI
Hijmans RJ. raster: Geographic data analysis and modeling. 2023. https://rspatial.org/raster/ https://rspatial.org/raster/
Hoover SER, Ladley JJ, Shchepetkina AA, Tisch M, Gieseg SP, Tylianakis JM. Warming, CO2, and nitrogen deposition interactively affect a plant-pollinator mutualism. Ecology Letters. 2012;15(3):227–234. doi: 10.1111/j.1461-0248.2011.01729.x. PubMed DOI
Hothorn T, Bretz F, Westfall P. Simultaneous inference in general parametric models. Biometrical Journal. 2008;50(3):346–363. doi: 10.1002/bimj.200810425. PubMed DOI
IPCC . IPCC Sixth Assessment Report. Geneva: IPCC; 2021. The physical science basis.
Kakani VG, Reddy KR, Koti S, Wallace TP, Prasad PVV, Reddy VR, Zhao D. Differences in in vitro pollen germination and pollen tube growth of cotton cultivars in response to high temperature. Annals of Botany. 2005;96(1):59–67. doi: 10.1093/aob/mci149. PubMed DOI PMC
Kaushal N, Bhandari K, Siddique KHM, Nayyar H. Food crops face rising temperatures: an overview of responses, adaptive mechanisms, and approaches to improve heat tolerance. Cogent Food & Agriculture. 2016;2(1):50. doi: 10.1080/23311932.2015.1134380. DOI
Lee J-Y, Marotzke J, Bala G, Cao L, Corti S, Dunne JP, Engelbrecht F, Fischer E, Fyfe JC, Jones C, Maycock A, Mutemi J, Ndiaye O, Panickal S, Zhou T, Milinski S, Yun K-S, Armour K, Bellouin N, Bethke I, Byrne MP, Cassou C, Chen D, Cherchi A, Christensen HM, Connors SL, Di Luca A, Drijfhout SS, Fletcher CG, Forster P, Garcia-Serrano J, Gillett NP, Kaufmann DS, Keller DP, Kravitz B, Li H, Liang Y, MacDougall AH, Malinina E, Menary M, Merryfield WJ, Min S-K, Nicholls ZRJ, Notz D, Pearson B, Priestley MDK, Quaas J, Ribes A, Ruane AC, Sallee J-B, Sanchez-Gomez E, Seneviratne SI, Slangen ABA, Smith C, Stuecker MF, Swaminathan R, Thorne PW, Tokarska KB, Toohey M, Turner A, Volpi D, Xiao C, Zappa G. Future global climate: scenario-based projections and near-term information. In: Masson-Delmotte V, Zhai P, Pirani A, Connors SL, Pean C, Berger S, Caud N, Chen Y, Goldfarb L, Gomis MI, Huang M, Leitzell K, Lonnoy E, Matthews JBR, Maycock TK, Waterfield T, Yelekçi O, Yu R, Zhou B, editors. Climate Change 2021: The Physical Science Basis. Contribution of Working Group I to the Sixth: Assessment Report of the Intergovernmental Panel on Climate Change. Geneva: IPCC; 2021.
Leech L, Simpson DW, Whitehouse AB. Effect of temperature and relative humidity on pollen germination in four strawberry cultivars. Acta Horticulturae. 2002;567:261–263. doi: 10.17660/ActaHortic.2002.567.53. DOI
Leimu R, Fischer M. A meta-analysis of local adaptation in plants. PLOS ONE. 2008;3(12):e4010. doi: 10.1371/journal.pone.0004010. PubMed DOI PMC
Lenoir J, Gégout JC, Marquet PA, de Ruffray P, Brisse H. A significant upward shift in plant species optimum elevation during the 20th century. Science. 2008;320(5884):1768–1771. doi: 10.1126/science.1156831. PubMed DOI
Lewis D. The physiology of incompatibility in plants-I. The effect of temperature. Proceedings of the Royal Society B: Biological Sciences. 1942;131(862):13–26. doi: 10.1098/rspb.1942.0015. DOI
Lohani N, Singh MB, Bhalla PL. High temperature susceptibility of sexual reproduction in crop plants. Journal of Experimental Botany. 2020;71(2):555–568. doi: 10.1093/jxb/erz426. PubMed DOI
Lohani N, Singh MB, Bhalla PL. Short-term heat stress during flowering results in a decline in canola seed productivity. Journal of Agronomy and Crop Science. 2022;208(4):486–496. doi: 10.1111/jac.12534. DOI
Lortie CJ, Hierro JL. A synthesis of local adaptation to climate through reciprocal common gardens. Journal of Ecology. 2022;110(5):1015–1021. doi: 10.1111/1365-2745.13664. DOI
Lovane M, Cirillo A, Izzo LG, Di Vaio C, Aronne G. High temperature and humidity affect pollen viability and longevity in Olea europaea L. Agronomy. 2021;12(1):1. doi: 10.3390/agronomy12010001. DOI
Macel M, Lawson CS, Mortimer SR, Šmilauerova M, Bischoff A, Crémieux L, Doležal J, Edwards AR, Lanta V, Bezemer TM, Van Der Putten WH, Igual JM, Rodriguez-Barrueco C, Müller-Schärer H, Steinger T. Climate vs. soil factors in local adaptation of two common plant species. Ecology. 2007;88:424–433. doi: 10.1890/0012-9658(2007)88[424:CVSFIL]2.0.CO;2. PubMed DOI
McKee J, Richards AJ. The Effect of temperature on reproduction in five Primula species. Annals of Botany. 1998;82(3):359–374. doi: 10.1006/anbo.1998.0697. DOI
Mesihovic A, Iannacone R, Firon N, Fragkostefanakis S. Heat stress regimes for the investigation of pollen thermotolerance in crop plants. Plant Reproduction. 2016;29(1–2):93–105. doi: 10.1007/s00497-016-0281-y. PubMed DOI
Müller F, Rieu I. Acclimation to high temperature during pollen development. Plant Reproduction. 2016;29(1–2):107–118. doi: 10.1007/s00497-016-0282-x. PubMed DOI PMC
Ollerton J, Winfree R, Tarrant S. How many flowering plants are pollinated by animals? Oikos. 2011;120(3):321–326. doi: 10.1111/j.1600-0706.2010.18644.x. DOI
Pham VT, Herrero M, Hormaza JI. Effect of temperature on pollen germination and pollen tube growth in longan (Dimocarpus longan Lour.) Scientia Horticulturae. 2015;197(1–2):470–475. doi: 10.1016/j.scienta.2015.10.007. DOI
Pigott CD, Huntley JP. Factors controlling the distribution of Tilia cordata at the northern limits of its geographical range. ii. history in North-West England. New Phytologist. 1980;84(1):145–164. doi: 10.1111/j.1469-8137.1980.tb00757.x. DOI
Poudel S, Vennam RR, Shrestha A, Reddy KR, Wijewardane NK, Reddy KN, Bheemanahalli R. Resilience of soybean cultivars to drought stress during flowering and early-seed setting stages. Scientific Reports. 2023;13(1):1277. doi: 10.1038/s41598-023-28354-0. PubMed DOI PMC
R Core Team . R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2022.
Rang ZW, Jagadish SVK, Zhou QM, Craufurd PQ, Heuer S. Effect of high temperature and water stress on pollen germination and spikelet fertility in rice. Environmental and Experimental Botany. 2011;70(1):58–65. doi: 10.1016/j.envexpbot.2010.08.009. DOI
Rao G, Ashraf U, Kong L, Mo Z, Xiao L, Zhong K, Rasul F, Tang X. Low soil temperature and drought stress conditions at flowering stage affect physiology and pollen traits of rice. Journal of Integrative Agriculture. 2019;18(8):1859–1870. doi: 10.1016/S2095-3119(18)62067-2. DOI
Rosbakh S, Pacini E, Nepi M, Poschlod P. An unexplored side of regeneration niche: seed quantity and quality are determined by the effect of temperature on pollen performance. Frontiers in Plant Science. 2018;9:1036. doi: 10.3389/fpls.2018.01036. PubMed DOI PMC
Rosbakh S, Poschlod P. Minimal temperature of pollen germination controls species distribution along a temperature gradient. Annals of Botany. 2016;117(7):1111–1120. doi: 10.1093/aob/mcw041. PubMed DOI PMC
Scherrer D, Korner C. Infra-red thermometry of alpine landscapes challenges climatic warming projections: thermometry of alpine landscapes. Global Change Biology: no-no. Global Change Biology. 2009;16(9):2602–2613. doi: 10.1111/j.1365-2486.2009.02122.x. DOI
Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, Tinevez J-Y, White DJ, Hartenstein V, Eliceiri K, Tomancak P, Cardona A. Fiji: an open-source platform for biological-image analysis. Nature Methods. 2012;9(7):676–682. doi: 10.1038/nmeth.2019. PubMed DOI PMC
Shi W, Li X, Schmidt RC, Struik PC, Yin X, Jagadish SVK. Pollen germination and in vivo fertilization in response to high-temperature during flowering in hybrid and inbred rice: rice pollen & in vivo fertilization under heat. Plant, Cell & Environment. 2018;41(6):1287–1297. doi: 10.1111/pce.13146. PubMed DOI
Sorkheh K, Shiran B, Rouhi V, Khodambashi M, Wolukau JN, Ercisli S. Response of in vitro pollen germination and pollen tube growth of almond (Prunus dulcis Mill.) to temperature, polyamines and polyamine synthesis inhibitor. Biochemical Systematics and Ecology. 2011;39(4–6):749–757. doi: 10.1016/j.bse.2011.06.015. DOI
Steinacher G, Wagner J. Effect of temperature on the progamic phase in high-mountain plants: temperature effects on the progamic phase in mountain plants. Plant Biology. 2012;14(2):295–305. doi: 10.1111/j.1438-8677.2011.00498.x. PubMed DOI
Sung D-Y, Kaplan F, Lee K-J, Guy CL. Acquired tolerance to temperature extremes. Trends in Plant Science. 2003;8(4):179–187. doi: 10.1016/S1360-1385(03)00047-5. PubMed DOI
Tushabe D, Rosbakh S. A compendium of in vitro germination media for pollen research. Frontiers in Plant Science. 2021;12:733. doi: 10.3389/fpls.2021.709945. PubMed DOI PMC
Wagner J, Gastl E, Kogler M, Scheiber M. Cold tolerance of the male gametophyte during germination and tube growth depends on the flowering time. Plants. 2016;6(4):2. doi: 10.3390/plants6010002. PubMed DOI PMC
Walters J, Isaacs R. Pollen germination and tube growth in northern highbush blueberry are inhibited by extreme heat. HortScience. 2023;58(6):635–642. doi: 10.21273/HORTSCI17075-23. DOI
Wang Y, Tao H, Tian B, Sheng D, Xu C, Zhou H, Huang S, Wang P. Flowering dynamics, pollen, and pistil contribution to grain yield in response to high temperature during maize flowering. Environmental and Experimental Botany. 2019;158:80–88. doi: 10.1016/j.envexpbot.2018.11.007. DOI
Yamori W, Hikosaka K, Way DA. Temperature response of photosynthesis in C3, C4, and CAM plants: temperature acclimation and temperature adaptation. Photosynthesis Research. 2014;119(1–2):101–117. doi: 10.1007/s11120-013-9874-6. PubMed DOI
Young LW, Wilen RW, Bonham-Smith PC. High temperature stress of Brassica napus during flowering reduces micro- and megagametophyte fertility, induces fruit abortion, and disrupts seed production. Journal of Experimental Botany. 2004;55(396):485–495. doi: 10.1093/jxb/erh038. PubMed DOI
Zinn KE, Tunc-Ozdemir M, Harper JF. Temperature stress and plant sexual reproduction: uncovering the weakest links. Journal of Experimental Botany. 2010;61(7):1959–1968. doi: 10.1093/jxb/erq053. PubMed DOI PMC
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