Abstract
Herbivory is a fundamental type of plant–animal interaction that presents substantial selection pressure on plants to replace lost tissues and to prevent subsequent losses in fitness. Apical herbivory, which entails removal or damage to the apical meristem, causes a change in plant architecture by disrupting the balance of hormones produced in part by the apical meristem. Therefore, for an annual semelparous plant, the ability to preserve reproductive success following damage (i.e., to tolerate damage) is largely dependent on the plant’s pre-damage investment into fitness and its regrowth pattern following damage. Using multiple regression analyses, we assessed the relationship of developmental and architectural traits of experimentally damaged plants relative to undamaged plants of 33 Arabidopsis thaliana genotypes that display a wide range of undamaged fitness and damage tolerance. Our analyses revealed evidence for an evolutionary bet-hedging strategy within a subset of genotypes to presumably maximize fitness under natural herbivory—genotypes with the greatest seed production when undamaged exhibited a significant reduction in seed yield when damaged, while genotypes with low undamaged seed production were the only genotypes whose seed yield increased when damaged. Patterns of endopolyploidy paralleled those of seed production, such that the increase in whole-plant ploidy by genome re-replication during growth/regrowth contributes to undamaged fitness, damage tolerance, and their trade-off. Overall, this study provides the first large-scale characterization of A. thaliana regrowth patterns and suggests that investment into fitness and endopolyploidy when undamaged may come at a cost to tolerance ability once damaged.
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References
Aarssen LW (1995) Hypotheses for the evolution of apical dominance in plants: implications for the interpretation of overcompensation. Oikos 74:149–156. doi:10.2307/3545684
Abbott RJ, Gomes MF (1988) Population genetic structure and outcrossing rate of Arabidopsis thaliana (L.) Heynh. Heredity 62:411–418. doi:10.1038/hdy.1989.56
Agrawal AA (1998) Induced responses to herbivory and increased plant performance. Science 279:1201–1202. doi:10.1126/science.279.5354.1201
Barow M (2006) Endopolyploidy in seed plants. BioEssays 28:271–281. doi:10.1002/bies.20371
Barow M, Meister A (2003) Endopolyploidy in seed plants is differently correlated systematics, organ, life strategy, and size. Plant Cell Environ 26:571–584. doi:10.1046/j.1365-3040.2003.00988.x
Barton KE (2016) Tougher and thornier: general patterns in the induction of physical defence traits. Funct Ecol 30(2):181–187. doi:10.1111/1365-2435.12495
Belsky AJ, Carson WP, Jensen CL, Fox GA (1993) Overcompensation by plants: herbivore optimization or red herring? Evol Ecol 7:109–121. doi:10.1007/BF01237737
Benner BL (1988) Effects of apex removal and nutrient supplementation on branching and seed production in Thlaspi arvense (Brassicaceae). Am J Bot 75(5):645–651. doi:10.2307/2444198
Bernier G, Périlleux C (2005) A physiological overview of the genetics of flowering time control. Plant Biotechnol J 3(1):3–16. doi:10.1111/j.1467-7652.2004.00114.x
Boege K, Marquis RJ (2005) Facing herbivory as you grow up: the ontogeny of resistance in plants. Trends Ecol Evol 20(8):441–448. doi:10.1016/j.tree.2005.05.001
Efron B (1983) Estimating the error rate of a prediction rule: improvement on cross-validation. J Am Stat Assoc 78:316–331. doi:10.2307/2288636
Fornoni J, Valverde PL, Núñez-Farfán J (2004) Population variation in the cost and benefit of tolerance and resistance against herbivory in Datura stramonium. Evolution 58:1696–1704. doi:10.1554/03-481
Galbraith DW, Harkins KR, Maddox JM, Ayres NM, Sharma DP, Firoozabady E (1983) Rapid flow cytometric analysis of the cell cycle in intact plant tissues. Science 220:1049–1051. doi:10.1126/science.220.4601.1049
Galbraith DW, Harkins KR, Knapp S (1991) Systemic endopolyploidy in Arabidopsis thaliana. Plant Physiol 96:985–989. doi:10.1104/pp.96.3.985
Gruntman M, Novoplansky A (2011) Ontogenetic contingency of tolerance mechanisms in response to apical damage. Ann Bot 108:965–973. doi:10.1093/aob/mcr204
Hawkes CV, Sullivan JJ (2001) The impact of herbivory on plants in different resource conditions: a meta-analysis. Ecology 82(7):20145–22058. doi:10.2307/2680068
Huhta A-K, Hellström K, Rautio P, Tuomi J (2000) A test of the compensatory continuum: fertilization increases and below-ground competition decreases the grazing tolerance of tall wormseed mustard (Erysimum strictum). Evol Ecol 14:353–372. doi:10.1023/A:1010808925284
Ishida T, Adachi S, Yoshimura M, Shimizu K, Umeda M, Sugimoto K (2010) Auxin modulates the transition from the mitotic cycle to the endocycle in Arabidopsis. Development 137:63–71. doi:10.1242/dev.035840
Juenger T, Lennartsson T (2000) Tolerance in plant ecology and evolution: toward a more unified theory of plant herbivore interactions. Evol Ecol 14:283–287. doi:10.1023/A:1017323621181
Keeley JE, Bond WJ (1999) Mast flowering and semelparity in bamboos: the bamboo fire cycle hypothesis. Am Nat 154(3):383–391. doi:10.1086/303243
Klinkhamer PGL, Kubo T, Iwasa Y (1997) Herbivores and the evolution of the semelparous perennial life-history of plants. J Evol Biol 10:529–550. doi:10.1046/j.1420-9101.1997.10040529.x
Knight TM (2003) Effects of herbivory and its timing across populations of Trillium grandiflorum (Liliaceae). Am J Bot 90:1207–1214. doi:10.3732/ajb.90.8.1207
Kowles RV, Phillips RL (1988) Endosperm development in maize. Int Rev Cytol 112:97–136
Larkins BA, Dilkes BP, Dante RA, Coelho CM, Woo YM, Liu Y (2001) Investigating the hows and whys of DNA endoreduplication. J Exp Bot 52:183–192. doi:10.1093/jexbot/52.355.183
Lee HO, Davidson JM, Duronio RJ (2009) Endoreplication: ploidy with purpose. Gene Dev 23:2461–2477. doi:10.1101/gad.1829209
Leitch AR, Leitch IJ (2012) Ecological and genetic factors linked to contrasting genome dynamics in seed plants. N Phytol 194:629–646. doi:10.1111/j.1469-8137.2012.04105.x
Lennartsson T, Nilsson P, Tuomi J (1997) Evidence for an evolutionary history of overcompensation in the grassland biennial Gentianella campestris (Gentianaceae). Am Nat 149:1147–1155. doi:10.1086/286043
Maschinski J, Whitham TG (1989) The continuum of plant responses to herbivory: the influence of plant association, nutrient availability, and timing. Am Nat 134:1–19. doi:10.1086/284962
Mattson WJ (1980) Herbivory in relation to plant nitrogen content. Annu Rev Ecol Syst 11:119–161. doi:10.1146/annurev.es.11.110180.001003
Mauricio R, Rausher MD, Burdick BS (1997) Variation in the defense strategies of plants: are resistant and tolerance mutually exclusive? Ecology 78:1301–1311. doi: 1890/0012-9658(1997)078[1301:VITDSO]2.0.CO;2
McNaughton SJ (1979) Grazing as an optimization process: grass-ungulate relationships in the Serengeti. Am Nat 113:691–703. doi:10.1086/283426
Mithöfer A, Boland W (2012) Plant defense against herbivores: chemical aspects. Annu Rev Plant Biol 63:431–450. doi:10.1146/annurev-arplant-042110-103854
Nagl W (1976) Endoreduplication and polyteny understood as evolutionary strategies. Nature 261:614–615. doi:10.1038/261614a0
Nagl W (1978) Endopolyploidy and polyteny in differentiation and evolution. North-Holland Publishing Company, North-Holland, Amsterdam
Nilsson P, Tuomi J, Åström M (1996) Bud dormancy as a bet-hedging strategy. Am Nat 147:269–281. doi:10.1086/285849
Núñez-Farfán J, Fornoni J, Valverde PL (2007) The evolution of resistance and tolerance to herbivores. Annu Rev Ecol Evol S 38:541–566. doi:10.1146/annurev.ecolsys.38.091206.095822
Paige KN, Whitham TG (1987) Overcompensation in response to mammalian herbivory: the advantage of being eaten. Am Nat 129:407–416
Pyke DA (1989) Limited resources and reproductive constraints in annuals. Funct Ecol 3:221–228. doi:10.2307/2389304
Rausher MD (1992) Natural selection and the evolution of plant–animal interactions. In: Roitberg BD, Isman MS (eds) Insect and chemical ecology: an evolutionary approach. Routledge, Chapman and Hall, New York, pp 20–80
Sachs T, Thimann KV (1967) The role of auxins and cytokinins in the release of buds from dominance. Am J Bot 54:136–144
Scholes DR, Paige KN (2011) Chromosomal plasticity: mitigating the impacts of herbivory. Ecology 92:1691–1698. doi:10.1890/10-2269.1
Scholes DR, Paige KN (2014) Plasticity in ploidy underlies plant fitness compensation to herbivore damage. Mol Ecol 23:4862–4870. doi:10.1111/mec.12894
Scholes DR, Paige KN (2015a) Plasticity in ploidy: a generalized response to stress. Trends Plant Sci 20:165–175. doi:10.1016/j.tplants.2014.11.007
Scholes DR, Paige KN (2015b) Transcriptomics of plant responses to apical damage reveals no negative correlation between tolerance and defense. Plant Ecol 216:1177–1190. doi:10.1007/s11258-015-0500-x
Scholes DR, Siddappaji MH, Paige KN (2013) The genetic basis of overcompensation in plants: a synthesis. Int J Mod Bot 3:34–42. doi:10.5923/s.ijmb.201310.05
Scholes DR, Wszalek AE, Paige KN (2016) Regrowth patterns and rosette attributes contribute to the differential compensatory responses of Arabidopsis thaliana genotypes to apical damage. Plant Biol 18:239–248. doi:10.1111/plb.12404
Scholes DR, Dalrymple J, Mesa JM, Banta JA, Paige KN (2017) An assessment of the molecular mechanisms contributing to tolerance to apical damage in natural populations of Arabidopsis thaliana. Plant Ecol 218:265–276. doi:10.1007/s11258-016-0685-7
Siddappaji MH, Scholes DR, Bohn MO, Paige KN (2013) Overcompensation in response to herbivory in Arabidopsis thaliana: the role of glucose-6-phosphate dehydrogenase and the oxidative pentose-phosphate pathway. Genetics 195:589–598. doi:10.1534/genetics.113.154351
Stowe KA, Marquis RJ, Hochwender CG, Simms EL (2000) The evolutionary ecology of tolerance to consumer damage. Annu Rev Ecol Syst 31:565–595. doi:10.1146/annurev.ecolsys.31.1.565
Strauss SY, Agrawal AA (1999) The ecology and evolution of plant tolerance to herbivory. Trends Ecol Evol 14:179–185. doi:10.1016/S0169-5347(98)01576-6
Sugimoto-Shirasu K, Roberts K (2003) “Big it up”: endoreduplication and cell-size control in plants. Curr Opin Plant Biol 6:544–553. doi:10.1016/j.pbi.2003.09.009
Tibshirani R (1996) Regression shrinkage and selection via the lasso. J Roy Stat Soc B 58:267–288. doi:10.2307/41262671
Tibshirani R (2011) Regression shrinkage and selection via the lasso: a retrospective. J R Stat Soc B 73:273–282. doi:10.1111/j.1467-9868.2011.00771.x
Tiffin P (2000) Mechanisms of tolerance to herbivore damage: what do we know? Evol Ecol 14:523–536. doi:10.1086/303271
Traas J, Hülskamp M, Gendreau E, Höfte H (1998) Endoreduplication and development: rule without dividing? Curr Opin Plant Biol 1:498–503. doi:10.1016/S1369-5266(98)80042-3
Tucker C, Avila-Sakar G (2010) Ontogenetic changes in tolerance to herbivory in Arabidopsis. Oecologia 164:1005–1015. doi:10.1093/aob/mct083
van der Meijden E, Wijn M, Verkaar HJ (1988) Defense and regrowth, alternative plant strategies in the struggle against herbivores. Oikos 51:355–363. doi:10.2307/3565318
Weinig C, Stinchombe JR, Schmitt J (2003) Evolutionary genetics of resistance and tolerance to natural herbivory in Arabidopsis thaliana. Evolution 57:1270–1280. doi:10.1554/02-469
Acknowledgements
Flow cytometry was performed by the Iowa State University Flow Cytometry Facility. Seeds were obtained from the Arabidopsis Biological Resource Center at The Ohio State University.
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DRS conducted plant growth, maintenance, and measurement. DRS, ENR, and KNP conducted study design, data analysis, and writing.
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This research was supported by awards from the National Science Foundation (DEB1146085 and associated REU) and the University of Illinois Campus Research Board to KNP.
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Communicated by Merijn Kant.
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Online Resource 1 (ESM1.pdf): Model iterations of LASSO regression of all traits and only architectural and developmental traits regressed against tolerance (Table 1), and regression of undamaged seed production vs. percent change in seed production for all genotypes combined and global ecotypes alone (Fig. 1)
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Scholes, D.R., Rasnick, E.N. & Paige, K.N. Characterization of Arabidopsis thaliana regrowth patterns suggests a trade-off between undamaged fitness and damage tolerance. Oecologia 184, 643–652 (2017). https://doi.org/10.1007/s00442-017-3897-1
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DOI: https://doi.org/10.1007/s00442-017-3897-1