The phenotypes of plants can be influenced by the environmental conditions experienced by their parents. However, there is still much uncertainty about how common and how predictable such parental environmental effects really are. We carried out a comprehensive experimental test for parental effects, subjecting plants of multiple Arabidopsis thaliana genotypes to 24 different biotic or abiotic stresses, or combinations thereof, and comparing their offspring phenotypes in a common environment. The majority of environmental stresses caused significant parental effects, with -35% to +38% changes in offspring fitness. The expression of parental effects was strongly genotype-dependent, and multiple environmental stresses often acted nonadditively when combined. The direction and magnitude of parental effects were unrelated to the direct effects on the parents: Some environmental stresses did not affect the parents but caused substantial effects on offspring, while for others, the situation was reversed. Our study demonstrates that parental environmental effects are common and often strong in A. thaliana, but they are genotype-dependent, act nonadditively, and are difficult to predict. We should thus be cautious with generalizing from simple studies with single plant genotypes and/or only few individual environmental stresses. A thorough and general understanding of parental effects requires large multifactorial experiments.

Department of Experimental Plant Ecology Radboud University PO Box 9100 6500 GL Nijmegen the Netherlands

Gregor Mendel Institute of Molecular Plant Biology Dr Bohr Gasse 3 1030 Vienna Austria

Institute of Biology University of Marburg Karl von Frisch Straße 8 35032 Marburg Germany

Institute of Botany of the CAS Zámek 1 252 43 Průhonice Czech Republic

Institute of Plant Breeding Seed Science and Population Genetics University of Hohenheim 70599 Stuttgart Germany

Institute of Plant Sciences University of Bern Altenbergrain 21 3013 Bern Switzerland

Key Laboratory of the Ministry of Education for Coastal and Wetland Ecosystems College of the Environment and Ecology Xiamen University Xiamen Fujian 361102 China

Plant Ecology and Nature Conservation Group Wageningen University PO Box 47 6700 AA Wageningen the Netherlands

Plant Evolutionary Ecology University of Tübingen Auf der Morgenstelle 5 72076 Tübingen Germany

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Agrawal AA. 2001. Transgenerational consequences of plant responses to herbivory: an adaptive maternal effect? The American Naturalist 157: 555-569.

Agrawal AA. 2002. Herbivory and maternal effects: mechanisms and consequences of transgenerational induced plant resistance. Ecology 83: 3408-3415.

Andalo C, Raquin C, Machon N, Godelle B, Mousseau M. 1998. Direct and maternal effects of elevated CO2 on early root growth of germinating Arabidopsis thaliana seedlings. Annals of Botany 81: 405-411.

Andalo S, Mazer SJ, Godelle B, Machon N. 1999. Parental environmental effects on life history traits in Arabidopsis thaliana (Brassicaceae). New Phytologist 142: 173-184.

Auge GA, Leverett LD, Edwards BR, Donohue K. 2017. Adjusting phenotypes via within- and across-generational plasticity. New Phytologist 216: 343-349.

Badyaev AV. 2008. Maternal effects as generators of evolutionary change: a reassessment. Annals of the New York Academy of Sciences 1133: 151-161.

Badyaev AV. 2009. Evolutionary significance of phenotypic accommodation in novel environments: an empirical test of the Baldwin effect. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 364: 1125-1141.

Badyaev AV, Uller T. 2009. Parental effects in ecology and evolution: mechanisms, processes and implications. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 364: 1169-1177.

Baker H, Sultan SE, Lopez-Ichikawa M, Waterman R. 2019. Transgenerational effects of parental light environment on progeny competitive performance and lifetime fitness. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 374: 20180182.

Blödner C, Goebel C, Feussner I, Gatz C, Polle A. 2007. Warm and cold parental reproductive environments affect seed properties, fitness, and cold responsiveness in Arabidopsis thaliana progenies. Plant, Cell & Environment 30: 165-175.

Bonduriansky R, Day T. 2009. Nongenetic inheritance and its evolutionary implications. Annual Review of Ecology, Evolution, and Systematics 40: 103-125.

Bossdorf O, Shuja Z, Banta JA. 2009. Genotype and maternal environment affect belowground interactions between Arabidopsis thaliana and its competitors. Oikos 118: 1541-1551.

Boyd EW, Dorn LA, Weinig C, Schmitt J. 2007. Maternal effects and germination timing mediate the expression of winter and spring annual life histories in Arabidopsis thaliana. International Journal of Plant Sciences 168: 205-214.

Burgess SC, Marshall DJ. 2011. Temperature-induced maternal effects and environmental predictability. Journal of Experimental Biology 214: 2329-2336.

Chevin LM, Lande R, Mace M. 2010. Adaptation, plasticity, and extinction in a changing environment: towards a predictive theory. PLoS Biology 8: e1000357.

Cipollini DF. 2002. Does competition magnify the fitness costs of induced responses in Arabidopsis thaliana? A manipulative approach. Oecologia 131: 514-520.

Colicchio J. 2017. Transgenerational effects alter plant defence and resistance in nature. Journal of Evolutionary Biology 30: 664-680.

Dyer AR, Brown CS, Espeland EK, McKay JK, Meimberg HM, Rice KJ. 2010. The role of adaptive trans-generational plasticity in biological invasions of plants. Evolutionary Applications 3: 179-192.

Elwell AL, Gronwall DS, Miller ND, Spalding EP, Brooks TLD. 2011. Separating parental environment from seed size effects on next generation growth and development in Arabidopsis. Plant, Cell & Environment 34: 291-301.

Falconer DS. 1965. Maternal effects and selection response. Genetics today. Proceeding of the XI International congress on genetics. Oxford: Pergamon.

Galloway LF. 2001. The effect of maternal and paternal environments on seed characters in the herbaceous plant Campanula americana. American Journal of Botany 88: 832-840.

Galloway LF, Etterson JR. 2007. Transgenerational plasticity is adaptive in wild. Science 318: 1134-1136.

González RAP, Dumalasová V, Rosenthal J, Skuhrovec J, Latzel V. 2017. The role of transgenerational effects in adaptation of clonal offspring of white clover (Trifolium repens) to drought and herbivory. Evolutionary Ecology 31: 345-361.

González RAP, Preite V, Verhoeven KJF, Latzel V. 2018. Transgenerational effects and epigenetic memory in the clonal plant Trifolium repens. Frontiers in Plant Science 9: 1677.

Groot MP, Kubisch A, Ouborg NJ, Pagel J, Schmid KJ, Vergeer P, Lampei C. 2017. Transgenerational effects of mild heat in Arabidopsis thaliana show strong genotype specificity that is explained by climate at origin. New Phytologist 215: 1221-1234.

He H, de Souza VD, Snoek LB, Schnabel S, Nijveen H, Hilhorst H, Bentsink L. 2014. Interaction between parental environment and genotype affects plant and seed performance in Arabidopsis. Journal of Experimental Biology 65: 6603-6615.

Herman JJ, Sultan SE. 2011. Adaptive transgenerational plasticity in plants: case studies, mechanisms, and implications for natural populations. Frontiers in Plant Science 2: 102.

Hof C, Araujo MB, Jetz W, Rahbek C. 2011. Additive threats from pathogens, climate and land-use change for global amphibian diversity. Nature 480: 516-519.

Hoffmann AA, Sgrò CM. 2011. Climate change and evolutionary adaptation. Nature 470: 479-485.

IPCC. 2021. Climate change: the physical science basis. In: Masson-Delmotte V, Zhai P, Pirani A, Connors SL, Péan C, Berger S, Caud N, Chen Y, Goldfarb L, Gomis MI et al., eds. Contribution of working group I to the sixth assessment report of the Intergovernmental Panel on Climate Change. Cambridge, UK: Cambridge University Press.

Jablonka E, Raz G. 2009. Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution. The Quarterly Review of Biology 84: 131-176.

Jump AS, Penuelas J. 2005. Running to stand still: adaptation and the response of plants to rapid climate change. Ecology Letters 8: 1010-1020.

Kirkpatrick M, Lande R. 1989. The evolution of maternal characters. Evolution 43: 485-503.

Kochanek J, Steadman KJ, Probert RJ, Adkins SW. 2013. Parental effects modulate seed longevity: exploring parental and offspring phenotypes to elucidate pre-zygotic environmental influences. New Phytologist 191: 223-233.

Laland KN, Uller T, Feldman MW, Sterelny K, Müller GB, Moczek A, Jablonka E, Odling-Smee J. 2015. The extended evolutionary synthesis: its structure, assumptions and predictions. Proceedings of the Royal Society B: Biological Sciences 282: 20151019.

Lampei C. 2019. Multiple simultaneous treatments change plant response from adaptive parental effects to within-generation plasticity, in Arabidopsis thaliana. Oikos 128: 368-379.

Latzel V. 2015. Pitfalls in ecological research - transgenerational effects. Folia Geobotanica 50: 75-85.

Latzel V, Hájek T, Klimešová J, Gómez S. 2009. Nutrients and disturbance history in two Plantago species: maternal effects as a clue for observed dichotomy between resprouting and seeding strategies. Oikos 118: 1669-1678.

Latzel V, Hájek T, Klimešová J, Gómez S, Šmilauer P. 2010. Maternal effects alter progeny's response to disturbance and nutrients in two Plantago species. Oikos 119: 1700-1710.

Latzel V, Janeček Š, Doležal J, Klimešová J, Bossdorf O. 2014. Adaptive transgenerational plasticity in the perennial Plantago lanceolata. Oikos 123: 41-46.

Lau JA, Peiffer J, Reich PB, Tiffin P. 2008. Transgenerational effects of global environmental change: long-term CO2 and nitrogen treatments influence offspring growth response to elevated CO2. Oecologia 158: 141-150.

Marshall DJ, Uller T. 2007. When is a maternal effect adaptive? Oikos 116: 1957-1963.

Meinke DW, Cherry JM, Dean C, Rounsley SD, Koornneef M. 1998. Arabidopsis thaliana: a model plant for genome analysis. Science 282: 662-682.

Münzbergová Z, Hadincová V, Skálová H, Vandvik V. 2017. Genetic differentiation and plasticity interact along temperature and precipitation gradients to determine plant performance under climate change. Journal of Ecology 105: 1358-1373.

Nicotra AB, Atkin OK, Bonser SP, Davidson AM, Finnegan J, Mathesius U, Poot P, Purugganan MD, Richards CL, Valladares F et al. 2010. Plant phenotypic plasticity in a changing climate. Trends in Plant Science 15: 1360-1385.

Niinemets Ü. 2010. Responses of forest trees to single and multiple environmental stresses from seedlings to mature plants: past stress history, stress interactions, tolerance and acclimation. Forest Ecology and Management 260: 1623-1639.

Pigliucci M. 2002. Ecology and evolutionary biology of Arabidopsis. The Arabidopsis book. American Society of Plant Biologists 1: e0003.

Pigliucci M, Murren CJ, Schlichting CD. 2006. Phenotypic plasticity and evolution by genetic assimilation. Journal of Experimental Biology 209: 2362-2367.

Puy J, de Bello F, Dvořáková H, Medina N, Latzel V, Carmona CP. 2021. Competition-induced transgenerational plasticity influences competitive interactions and leaf decomposition of offspring. New Phytologist 229: 3497-3507.

R Core Team. 2021. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. [WWW document] URL https://www.R-project.org/ [accessed 20 October 2022].

Räsänen K, Kruuk LEB. 2007. Maternal effects and evolution at ecological time-scales. Functional Ecology 21: 408-421.

Rasmussen S, Barah PJ, Suarez-Rodriguez MC, Bressendorff S, Friis P, Costantino P, Bones AM, Nielsen HB, Mund J. 2013. Transcriptome responses to combinations of stresses in Arabidopsis. Plant Physiology 161: 1783-1794.

Richards CL, Alonso C, Becker V, Bossdorf O, Bucher E, Colomé-Tatché M, Durka W, Engelhardt J, Gaspar B, Gogol-Döring A et al. 2017. Ecological plant epigenetics: evidence from model and non-model species, and the way forward. Ecology Letters 20: 1576-1590.

Riginos C, Heschel MS, Schmitt J. 2007. Maternal effects of drought stress and inbreeding in Impatiens capensis (Balsaminaceae). American Journal of Botany 94: 1984-1991.

Shaw MR, Zavaleta ES, Chiariello NR, Cleland EE, Mooney HA, Field CB. 2002. Grassland responses to global environmental changes suppressed by elevated CO2. Science 298: 1987-1990.

Shears NT, Ross PM. 2010. Toxic cascades: multiple anthropogenic stressors have complex and unanticipated interactive effects on temperate reefs. Ecology Letters 13: 1149-1159.

Stinchcombe JR, Caicedo AL, Hopkins R, Mays C, Boyd EW, Purugganan MD, Schmitt J. 2005. Vernalization sensitivity in Arabidopsis thaliana (Brassicaceae): the effects of latitude and FLC variation. American Journal of Botany 92: 1701-1707.

Storey JD, Bass AJ, Dabney A, Robinson D. 2022. qvalue: Q-value estimation for false discovery rate control. [WWW document] URL http://github.com/jdstorey/qvalue [accessed 20 October 2022].

Sultan SE. 2000. Phenotypic plasticity for plant development, function and life history. Trends in Plant Science 5: 537-542.

Sultan SE, Barton K, Wilczek AM. 2009. Contrasting patterns of transgenerational plasticity in ecologically distinct congeners. Ecology 90: 1831-1839.

Suter L, Widmer A. 2013a. Phenotypic effects of salt and heat stress over three generations in Arabidopsis thaliana. PLoS ONE 8: e80819.

Suter L, Widmer A. 2013b. Environmental heat and salt stress induce transgenerational phenotypic changes in Arabidopsis thaliana. PLoS ONE 8: e60364.

Tylianakis J, Didham RK, Bascompte J, Wardle DA. 2008. Global change and species interactions in terrestrial ecosystems. Ecology Letters 11: 1351-1363.

Vu WT, Chang PL, Moriuchi KS, Friesen ML. 2015. Genetic variation of transgenerational plasticity of offspring germination in response to salinity stress and the seed transcriptome of Medicago truncatula. BMC Ecology and Evolution 15: 59.

Whittle CA, Otto SP, Johnston MO, Krochko JE. 2009. Adaptive epigenetic memory of ancestral temperature regime in Arabidopsis thaliana. Botany 87: 650-657.

Yin J, Zhou M, Lin Z, Li QQ, Zhang YY. 2019. Transgenerational effects benefit offspring across diverse environments: a meta-analysis in plants and animals. Ecology Letters 22: 1976-1986.

Zandalinas SI, Fritschi FB, Mittler R. 2021. Global warming, climate change, and environmental pollution: recipe for a multifactorial stress combination disaster. Trends in Plant Science 26: 6.

Zhang H, Sonnewald U. 2017. Differences and commonalities of plant responses to single and combined stresses. The Plant Journal 90: 839-855.

Stronger transgenerational plasticity in clonal compared to sexual offspring of Fragaria vesca: effects of drought, elevated temperature and CO2

Environment-induced heritable variations are common in Arabidopsis thaliana

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Dryad
10.5061/dryad.wm37pvmrc