Plant mating systems affect adaptive plasticity in response to herbivory

Plant Journal

Volumn 78, Issue 3, 2014, Pages 481-490

  Campbell, Stuart A ^a,b   Halitschke, Rayko ^a   Thaler, Jennifer S ^a   Kessler, André ^a  

^a Department of Molecular Biology and Genetics   (United States)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

inbreeding depression; induced responses; mating systems; phytohormone; plant resistance; plant tolerance; Solanum carolinense

Indexed keywords

BIOLOGY; PLANTS (BOTANY);

INBREEDING DEPRESSION; INDUCED RESPONSES; MATING SYSTEM; PHYTOHORMONE; PLANT RESISTANCE; PLANT TOLERANCE; SOLANUM CAROLINENSE;

ECOLOGY;

PHYTOHORMONE;

ADAPTATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HERBIVORY; INBREEDING; METABOLISM; PHYSIOLOGY; REPRODUCTION; SOLANUM;

ADAPTATION, PHYSIOLOGICAL; HERBIVORY; INBREEDING; PLANT GROWTH REGULATORS; REPRODUCTION; SOLANUM;

EID: 84899495381     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12492     Document Type: Article

References (74)

1. Agrawal, A.A., Strauss, S.Y., and, Stout, M.J., (1999) Costs of induced responses and tolerance to herbivory in male and female fitness components of wild radish. Evolution, 53, 1093-1104.
2. Arney, S.E., and, Mitchell, D.L., (1969) Effect of abscisic acid on stem elongation and correlative inhibition. New Phytol. 68, 1001-1015.
3. Auld, J.R., and, Relyea, R.A., (2010) Inbreeding depression in adaptive plasticity under predation risk in a freshwater snail. Biol. Lett. 6, 222-224.
4. Babst, B.A., Ferrieri, R.A., Gray, D.W., Lerdau, M., Schlyer, D.J., Schueller, M., Thorpe, M.R., and, Orians, C.M., (2005) Jasmonic acid induces rapid changes in carbon transport and partitioning in Populus. New Phytol. 167, 63-72.
5. Baldwin, I.T., (1998) Jasmonate-induced responses are costly but benefit plants under attack in native populations. Proc. Natl Acad. Sci. USA, 95, 8113-8118.
6. Bello-Bedoy, R., and, Núñez-Farfán, J., (2011) The effect of inbreeding on defence against multiple enemies in Datura stramonium. J. Evol. Biol. 24, 518-530.
7. Campbell, S.A., and, Kessler, A., (2013) Plant mating system transitions drive the macroevolution of defense strategies. Proc. Natl Acad. Sci. USA, 110, 3973-3978.
8. Campbell, S.A., Thaler, J.S., and, Kessler, A., (2013) Plant chemistry underlies herbivore-mediated inbreeding depression in nature. Ecol. Lett. 16, 252-260.
9. Carr, D.E., and, Eubanks, M.D., (2002) Inbreeding alters resistance to insect herbivory and host plant quality in Mimulus guttatus (Scrophulariaceae). Evolution, 56, 22-30.
10. Chandler, P.M., and, Robertson, M., (1994) Gene expression regulated by abscisic acid and its relation to stress tolerance. Annu. Rev. Plant Physiol. Plant Mol. Biol. 45, 113-141.
11. Charlesworth, D., and, Charlesworth, B., (1987) Inbreeding depression and its evolutionary consequences. Annu. Rev. Ecol. Syst. 18, 237-268.
12. Charlesworth, B., and, Charlesworth, D., (1999) The genetic basis of inbreeding depression. Genet. Res. 74, 329-340.
13. Cheptou, P.O., and, Donohue, K., (2011) Environment-dependent inbreeding depression: its ecological and evolutionary significance. New Phytol. 189, 395-407.
14. Cheverud, J.M., (1996) Quantitative genetic analysis of cranial morphology in the cotton-top (Saguinus oedipus) and saddle-back (S. fuscicollis) tamarins. J. Evol. Biol. 9, 5-42.
15. Cheverud, J.M., and, Marroig, G., (2007) Comparing covariance matrices: random skewers method compared to the common principal components model. Genet. Mol. Biol. 30, 461-469.
16. Chevin, L.M., and, Lande, R., (2011) Adaptation to marginal habitats by evolution of increased phenotypic plasticity. J. Evol. Biol. 24, 1462-1476.
17. Chevin, L.M., Lande, R., and, Mace, G.M., (2010) Adaptation, plasticity, and extinction in a changing environment: towards a predictive theory. PLoS Biol. 8, e1000357.
18. Creelman, R.A., and, Mullet, J.E., (1997) Biosynthesis and action of jasmonates in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, 355-381.
19. Darwin, C., (1876) The Effects of Cross and Self Fertilisation in the Vegetable Kingdom. London: J. Murray.
20. Delphia, C.M., De Moraes, C.M., Stephenson, A.G., and, Mescher, M.C., (2009) Inbreeding in horsenettle influences herbivore resistance. Ecol. Entomol. 34, 513-519.
21. Deng, H.W., (1997) Increase in developmental instability upon inbreeding in Daphnia. Heredity, 78, 182-189.
22. Du, D.L., Winsor, J.A., Smith, M., Denicco, A., and, Stephenson, A.G., (2008) Resistance and tolerance to herbivory changes with inbreeding and ontogeny in a wild gourd (Cucurbitaceae). Am. J. Bot. 95, 84-92.
23. Eckert, C.G., Kalisz, S., Geber, M.A., et al,. (2010) Plant mating systems in a changing world. Trends Ecol. Evol. 25, 35-43.
24. Ellison, A., Cable, J., and, Consuegra, S., (2011) Best of both worlds? Association between outcrossing and parasite loads in a selfing fish. Evolution, 65, 3021-3026.
25. Fischer, M., van Kleunen, M., and, Schmid, B., (2000) Genetic Allee effects on performance, plasticity and developmental stability in a clonal plant. Ecol. Lett. 3, 530-539.
26. Gõmez, S., Ferrieri, R.A., Schueller, M., and, Orians, C.M., (2010) Methyl jasmonate elicits rapid changes in carbon and nitrogen dynamics in tomato. New Phytol. 188, 835-844.
27. Hauser, T.P., and, Loeschcke, V., (1996) Drought stress and inbreeding depression in Lychnis flos-cuculi (Caryophyllaceae). Evolution, 50, 1119-1126.
28. Heil, M., and, Baldwin, I.T., (2002) Fitness costs of induced resistance: emerging experimental support for a slippery concept. Trends Plant Sci. 7, 61-67.
29. Husband, B.C., and, Schemske, D.W., (1996) Evolution of the magnitude and timing of inbreeding depression in plants. Evolution, 50, 54-70.
30. Ivey, C.T., and, Carr, D.E., (2012) Tests for the joint evolution of mating system and drought escape in Mimulus. Ann. Bot. 109, 583-598. Erratum Ann. Bot. 109, 1381.
31. Ivey, C.T., Carr, D.E., and, Eubanks, M.D., (2004) Effects of inbreeding in Mimulus guttatus on tolerance to herbivory in natural environments. Ecology, 85, 567-574.
32. Karban, R., and, Baldwin, I., (1997) Induced Responses to Herbivory. Chicago, IL: University of Chicago Press.
33. Kariyat, R.R., Scanlon, S.R., Mescher, M.C., De Moraes, C.M., and, Stephenson, A.G., (2011) Inbreeding depression in Solanum carolinense (Solanaceae) under field conditions and implications for mating system evolution. PLoS One, 6, 7.
34. Kariyat, R.R., Mauck, K.E., Moraes, C.M., Stephenson, A.G., and, Mescher, M.C., (2012) Inbreeding alters volatile signalling phenotypes and influences tri-trophic interactions in horsenettle (Solanum carolinense L.). Ecol. Lett. 15, 301-309.
35. Kariyat, R.R., Balogh, C.M., Moraski, R.P., De Moraes, C.M., Mescher, M.C., and, Stephenson, A.G., (2013) Constitutive and herbivore-induced structural defenses are compromised by inbreeding in Solanum carolinense (Solanaceae). Am. J. Bot. 100, 1014-1021.
36. Keinanen, M., Oldham, N.J., and, Baldwin, I.T., (2001) Rapid HPLC screening of jasmonate-induced increases in tobacco alkaloids, phenolics, and diterpene glycosides in Nicotiana attenuata. J. Agric. Food Chem. 49, 3553-3558.
37. Kessler, A., and, Baldwin, I.T., (2002) Plant responses to insect herbivory: the emerging molecular analysis. Annu. Rev. Plant Biol. 53, 299-328.
38. Knight, T.A., (1799) An account of some experiments on the fecundation of vegetables. Philos. Trans. R. Soc. Lond. 89, 195-204.
39. Korpita, T., Gõmez, S., and, Orians, C.M., (2014) Cues from a specialist herbivore increase tolerance to defoliation in tomato. Func. Ecol. 28, 395-401.
40. Kristensen, T.N., Barker, J.S.F., Pedersen, K.S., and, Loeschcke, V., (2008) Extreme temperatures increase the deleterious consequences of inbreeding under laboratory and semi-natural conditions. Proc. Biol. Sci. 275, 2055-2061.
41. Lande, R., (1988) Genetics and demography in biological conservation. Science, 241, 1455-1460.
42. Lande, R., and, Schemske, D.W., (1985) The evolution of self-fertilization and inbreeding depression in plants. 1. Genetic models. Evolution, 39, 24-40.
43. Leimu, R., Kloss, L., and, Fischer, M., (2008) Effects of experimental inbreeding on herbivore resistance and plant fitness: the role of history of inbreeding, herbivory and abiotic factors. Ecol. Lett. 11, 1101-1110.
44. Leimu, R., Kloss, L., and, Fischer, M., (2012a) Inbreeding alters activities of the stress-related enzymes chitinases and β-1,3-glucanases. PLoS One, 7, e42326.
45. Leimu, R., Muola, A., Laukkanen, L., Kalske, A., Prill, N., and, Mutikainen, P., (2012b) Plant-herbivore coevolution in a changing world. Entomol. Exp. Appl. 144, 3-13.
46. Levin, D.A., (1970) Developmental instability and evolution in peripheral isolates. Am. Nat. 104, 343-353.
47. Lloyd, D.G., (1979) Some reproductive factors affecting the selection of self-fertilization in plants. Am. Nat. 113, 67-79.
48. Machado, R.A.R., Ferrieri, A.P., Robert, C.A.M., Glauser, G., Kallenbach, M., Baldwin, I.T., and, Erb, M., (2013) Leaf-herbivore attack reduces carbon reserves and regrowth from the roots via jasmonate and auxin signaling. New Phytol. 200, 1234-1246.
49. McCall, A.C., and, Carr, D.E., (2013) Does inbreeding affect tolerance to inflorescence damage in Mimulus guttatus?. Open Ecol. J. 6, 1-6.
50. Mithöfer, A., and, Boland, W., (2011) Plant defense against herbivores: chemical aspects. Annu. Rev. Plant Biol. 63, 431-450.
51. Murren, C.J., and, Dudash, M.R., (2012) Variation in inbreeding depression and plasticity across native and non-native field environments. Ann. Bot. 109, 621-632.
52. Norman, J.K., Sakai, A.K., Weller, S.G., and, Dawson, T.E., (1995) Inbreeding depression in morphological and physiological traits of Schiedea lydgatei (Caryophyllaceae) in two environments. Evolution, 49, 297-306.
53. Núñez-Farfán, J., Fornoni, J., and, Valverde, P.L., (2007) The evolution of resistance and tolerance to herbivores. Annu. Rev. Ecol. Evol. Syst. 38, 541-566.
54. O'Halloran, L.R., and, Carr, D.E., (2010) Phenotypic plasticity and inbreeding depression in Mimulus ringens (Phrymaceae). Evol. Ecol. Res. 12, 617-632.
55. Onkokesung, N., Galis, I., von Dahl, C.C., Matsuoka, K., Saluz, H.P., and, Baldwin, I.T., (2010) Jasmonic acid and ethylene modulate local responses to wounding and simulated herbivory in Nicotiana attenuata leaves. Plant Physiol. 153, 785-798.
56. Peña-Cortés, H., Fisahn, J., and, Willmitzer, L., (1995) Signals involved in wound-induced proteinase inhibitor II gene expression in tomato and potato plants. Proc. Natl Acad. Sci. USA, 92, 4106-4113.
57. Robert-Seilaniantz, A., Grant, M., and, Jones, J.D.G., (2011) Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annu. Rev. Phytopathol. 49, 317-343.
58. Rood, S.B., Buzzell, R.I., Mander, L.N., Pearce, D., and, Pharis, R.P., (1988) Gibberellins: a phytohormonal basis for heterosis in maize. Science, 241, 1216-1218.
59. Schlichting, C.D., (1986) The evolution of phenotypic plasticity in plants. Annu. Rev. Ecol. Syst. 17, 667-693.
60. Schlichting, C.D., and, Levin, D.A., (1986) Effects of inbreeding on phenotypic plasticity in cultivated Phlox. Theor. Appl. Genet. 72, 114-119.
61. Schmelz, E.A., Engelberth, J., Alborn, H.T., O'Donnell, P., Sammons, M., Toshima, H., and, Tumlinson, J.H., (2003) Simultaneous analysis of phytohormones, phytotoxins, and volatile organic compounds in plants. Proc. Natl Acad. Sci. USA, 100, 10552-10557.
62. Schmitt, J., and, Ehrhardt, D.W., (1990) Enhancement of inbreeding depression by dominance and suppression in Impatiens capensis. Evolution, 44, 269-278.
63. Schwachtje, J., Minchin, P.E.H., Jahnke, S., van Dongen, J.T., Schittko, U., and, Baldwin, I.T., (2006) SNF1-related kinases allow plants to tolerate herbivory by allocating carbon to roots. Proc. Natl Acad. Sci. USA, 103, 12935-12940.
64. Sexton, J.P., McIntyre, P.J., Angert, A.L., and, Rice, K.J., (2009) Evolution and ecology of species range limits. Annu. Rev. Ecol. Evol. Syst. 40, 415-436.
65. Siikamaki, P., and, Lammi, A., (1998) Fluctuating asymmetry in central and marginal populations of Lychnis viscaria in relation to genetic and environmental factors. Evolution, 52, 1285-1292.
66. Steets, J.A., Wolf, D.E., Auld, J.R., and, Ashman, T.L., (2007) The role of natural enemies in the expression and evolution of mixed mating in hermaphroditic plants and animals. Evolution, 61, 2043-2055.
67. Stephenson, A.G., Leyshon, B., Travers, S.E., Hayes, C.N., and, Winsor, J.A., (2004) Interrelationships among inbreeding, herbivory, and disease on reproduction in a wild gourd. Ecology, 85, 3023-3034.
68. Stowe, K.A., Marquis, R.J., Hochwender, C.G., and, Simms, E.L., (2000) The evolutionary ecology of tolerance to consumer damage. Annu. Rev. Ecol. Evol. Syst. 31, 565-595.
69. Thaler, J.S., and, Bostock, R.M., (2004) Interactions between abscisic-acid-mediated responses and plant resistance to pathogens and insects. Ecology, 85, 48-58.
70. Thaler, J.S., Agrawal, A.A., and, Halitschke, R., (2010) Salicylate-mediated interactions between pathogens and herbivores. Ecology, 91, 1075-1082.
71. Thaler, J.S., Humphrey, P.T., and, Whiteman, N.K., (2012) Evolution of jasmonate and salicylate signal crosstalk. Trends Plant Sci. 17, 260-270.
72. Winn, A.A., Elle, E., Kalisz, S., et al. (2011) Analysis of inbreeding depression in mixed-mating plants provides evidence for selective interferance and stable mixed mating. Evolution, 65, 3339-3359.
73. Woodward, A.W., and, Bartel, B., (2005) Auxin: regulation, action, and interaction. Ann. Bot. 95, 707-735.
74. Zavala, J.A., and, Baldwin, I.T., (2006) Jasmonic acid signalling and herbivore resistance traits constrain regrowth after herbivore attack in Nicotiana attenuata. Plant Cell Environ. 29, 1751-1760.