Abstract
Herbivory imposes substantial selection pressure on plants, with the ability to regrow and maintain reproductive success a challenging but often necessary response by the plant. Despite the commonness of herbivore-induced damage, vast variation in tolerance ability exists among plants. Recent studies have suggested the role of endoreduplication (increasing ploidy within an individual) and the pentose phosphate pathway (a metabolic pathway that supports both primary and secondary metabolism) in contributing to the variation in tolerance ability among genotypes of Arabidopsis thaliana. We measured natural variation in apical meristem damage frequency, endoreduplication, and the sequence of G6PD1, an important gene in the pentose phosphate pathway, and related them to variation in tolerance of natural populations of A. thaliana over a portion of its native European range. Variation among populations in tolerance was significantly positively related to damage frequency, suggesting the potential for directional selection for tolerance ability as a product of damage frequency. We also discovered likely loss-of-function G6PD1 alleles in two populations, both of which displayed among the lowest levels of tolerance of all populations assessed. In addition, populations with the greatest increase in endopolyploidy also had the greatest ability to tolerate damage while populations with the greatest reduction in endopolyploidy had the lowest ability to tolerate damage. This study provides an assessment of variation in tolerance, damage frequency, G6PD1 sequence, and endopolyploidy in natural populations of A. thaliana, and also contributes to the growing body of research on the contributions of these specific molecular mechanisms to the tolerance response.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abbot RJ, Gomes MF (1987) Outcrossing rates in natural populations of Arabidopsis thaliana. Arabidopsis Inf Serv 25:85–88
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
Arendt J, Reznick D (2008) Convergence and parallelism reconsidered: what have we learned about the genetics of adaptation? Trends Ecol Evol 23:26–32. doi:10.1016/j.tree.2007.09.011
Asyraf M, Crawley MJ (2014) Effect of defoliation treatment on Mimosa pigra L. seedling survivability and resilience. Wetlands Ecol Manag 22:419–426. doi:10.1007/s11273-014-9343-9
Banta J, Stevens MHH, Pigliucci M (2010) A comprehensive test of the “limiting resources” framework applied to plant tolerance to apical meristem damage. Oikos 119:359–369. doi:10.1111/j.1600-0706.2009.17726.x
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 75:645–651. doi:10.2307/2444198
Brodsky WY, Uryvaeva IV (1977) Cell polyploidy: its relation to tissue growth and function. Int Rev Cytol 50:275–332. doi:10.1016/S0074-7696(08)60100-X
Bulleri F, Malquori F (2015) High tolerance to simulated herbivory in the clonal seaweed, Caulerpa cylindracea. Mar Environ Res 107:61–65. doi:10.1016/j.marenvres.2015.04.004
Cohen J (1992) A power primer. Psychol Bull 112:155–159. doi:10.1037/0033-2909.112.1.155
Ewing B, Green P (1998) Base-calling of automated sequencer traces using Phred. II. Error probabilities. Genome Res 8:186–194. doi:10.1101/gr.8.3.186
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
Godspeed D, Chehab EW, Min-Venditti A, Braam J, Covington MF (2012) Arabidopsis synchronizes jasmonate-mediated defense with insect circadian behavior. Proc Natl Acad Sci USA 109:4674–4677. doi:10.1073/pnas.111636810
Huhta AP, Lennartsson T, Tuomi J, Rautio P, Laine K (2000) Tolerance of Gentianella campestris in relation to damage intensity: an interplay between apical dominance and herbivory. Evol Ecol 14:373–392. doi:10.1023/A:1011028722860
Jones ME (1971) The population genetics of Arabidopsis thaliana. I. The breeding system. Heredity 27:39–50. doi:10.1038/hdy.1971.70
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
Kelley JL, Stinchcombe JR, Weinig C, Schmitt J (2005) Soft and hard selection on plant defence traits in Arabidopsis thaliana. Evol Ecol Res 7:287–302
Koornneef M, Alonso-Blanco C, Vreugdenhil D (2004) Naturally occurring genetic variation in Arabidopsis thaliana. Annu Rev Plant Biol 55:141–172. doi:10.1146/annurev.arplant.55.031903.141605
Kruger JN, von Schaewen A (2003) The oxidative pentose phosphate pathway: structure and organization. Curr Opin Plant Biol 6:236–246. doi:10.1016/S1369-5266(03)00039-6
Kuittinen H, Mattila A, Savolainen O (1997) Genetic variation at marker loci and in quantitative traits in natural populations in Arabidopsis thaliana. Heredity 79:144–152. doi:10.1038/hdy.1997.137
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948. doi:10.1093/bioinformatics/btm404
Lawrence MJ (1976) Variations in natural populations of Arabidopsis thaliana (L.) Heynh. In: Vaughan JG, Macleod AJ, Jones BMG (eds) The biology and chemistry of the Cruciferae. Academic, New York, pp 167–190
Lee HO, Davidson JM, Duronio RJ (2009) Endoreplication: ploidy with purpose. Gene Dev 23:2461–2477. doi:10.1101/gad.1829209
Lennartsson T, Tuomi J, Nilsson P (1997) Evidence for an evolutionary history of overcompensation in the grassland biennial Gentianella campestris (Gentianaceae). Am Nat 149:1147–1155. doi:10.1086/286043
Marquis RJ (1992) The selective impact of herbivores. In: Fritz RS, Simms EL (eds) Plant resistance to herbivores and pathogens: ecology, evolution and genetics. Chicago University Press, Chicago, pp 301–325
Martin LJ (2015) Historically browsed jewelweed populations exhibit greater tolerance to deer herbivory than historically protected populations. J Ecol 103:243–249. doi:10.1111/1365-2745.12344
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 DS (1997) Variation in the defense strategies of plants: are resistance and tolerance mutually exclusive? Ecology 78:1301–1311. doi:10.1890/0012-9658(1997)078[1301:VITDSO]2.0.CO;2
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, Amsterdam
Paige KN, Whitham TG (1987) Overcompensation in response to mammalian herbivory: the advantage of being eaten. Am Nat 129:407–416
Painter R (1958) Resistance of plants to insects. Annu Rev Entomol 3:267–290. doi:10.1146/annurev.en.03.010158.001411
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, New York, pp 20–88
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 216:1077–1090. 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
Siddappaji MH, Scholes DR, Bohn M, 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
Snape JW, Lawrence MJ (1971) The breeding system of Arabidopsis thaliana. Heredity 27:299–302. doi:10.1038/hdy.1971.91
Sokal RR, Rohlf FJ (1995) Biometry. WH Freeman & Co., New York
Stowe KA, Marquis RJ, Hockwender 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
Thimann KV, Skoog F (1934) On the inhibition of bud development and other functions of growth substance in Vicia faba. Proc R Soc 114:317–339. doi:10.1098/rspb.1934.0010
Tiffin P, Rausher M (1999) Genetic constraints and selection acting on tolerance to herbivory in the common morning glory Ipomoea purpurea. Am Nat 154:700–716. doi:10.1086/303271
Trnen L, Skárova M, Relichov J, Cetl I (1987) High outcrossing rates in a partially fertile line and their significance in the genetic structure of populations in Arabidopsis thaliana (L.) Heynh. Arabidopsis Inf Serv 23:31–40
van der Meijden E, Wijn M, Verkaar H (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
Wilkinson L (1999) Statistical methods in psychology journals: guidelines and explanations. Am Psychol 5:594–604. doi:10.1037/0003-066X.54.8.594
Wise MJ, Abrahamson WG (2007) Effects of resource availability on tolerance to herbivory: a review and assessment of three opposing models. Am Nat 169:443–454. doi:10.1086/512044
Wise MJ, Abrahamson WG (2008) Applying the limiting resource model to plant tolerance to apical meristem damage. Am Nat 172:635–647. doi:10.1086/591691
Acknowledgements
We thank the Iowa State Flow Cytometry Facility for measuring endopolyploidy and the University of Illinois High-Throughput Sequencing and Genotyping Unit of the Roy J. Carver Biotechnology for sequencing our samples. Jacqui Shykoff of the Université Paris-Sud provided assistance in locating natural A. thaliana populations. This study was funded by a Grant from the National Science Foundation (DEB—ROA #1146085) to KNP.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by William E. Rogers.
Electronic supplementary material
Below is the link to the electronic supplementary material.
11258_2016_685_MOESM1_ESM.pdf
Online Resource 1: Regressions of the percent change in cycle value vs. the frequency of apical meristem damage (Fig. 1a) and vs. tolerance (Fig. 1b); Alignment of G6PD1 protein sequences (Fig. 2) (ESM_1.pdf) (PDF 1046 kb)
Rights and permissions
About this article
Cite this article
Scholes, D.R., Dalrymple, J., Mesa, J.M. et al. An assessment of the molecular mechanisms contributing to tolerance to apical damage in natural populations of Arabidopsis thaliana . Plant Ecol 218, 265–276 (2017). https://doi.org/10.1007/s11258-016-0685-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11258-016-0685-7