Constitutive and herbivore-induced structural defenses are compromised by inbreeding in Solanum Carolinense (Solanaceae)

American Journal of Botany

Volumn 100, Issue 6, 2013, Pages 1014-1021

  Kariyat, Rupesh R ^a   Balogh, Christopher M ^a   Moraski, Ryan P ^a   de Moraes, Consuelo M ^a   Mescher, Mark C ^a   Stephenson, Andrew G ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

Herbivory; Horsenettle; Inbreeding; Induction; Mechanical damage; Solanaceae; Solanum carolinense; Spines; Structural defenses; Trichomes

Indexed keywords

DAMAGE; FLOWER; HERBIVORE; INBREEDING; INTERSPECIFIC INTERACTION; PEST DAMAGE; PLANT DEFENSE;

ANIMAL; ARTICLE; GENETICS; HERBIVORY; HISTOLOGY; HORSENETTLE; INBREEDING; INDUCTION; LARVA; MANDUCA; MECHANICAL DAMAGE; PHYSIOLOGY; PLANT LEAF; SOLANACEAE; SOLANUM; SOLANUM CAROLINENSE; SPINES; STRUCTURAL DEFENSES; TRICHOMES;

HERBIVORY; HORSENETTLE; INBREEDING; INDUCTION; MECHANICAL DAMAGE; SOLANACEAE; SOLANUM CAROLINENSE; SPINES; STRUCTURAL DEFENSES; TRICHOMES;

ANIMALS; HERBIVORY; INBREEDING; LARVA; MANDUCA; PLANT LEAVES; SOLANUM;

HEXAPODA; MANDUCA SEXTA; SOLANACEAE; SOLANUM CAROLINENSE;

EID: 84878871617     PISSN: 00029122     EISSN: None     Source Type: Journal    
DOI: 10.3732/ajb.1200612     Document Type: Article

References (69)

1. Agren J and D. W. Schemske. 1993. Outcrossing rate and inbreeding depression in two annual monoecious herbs, Begonia hirsuta and B. semiovata. Evolution; International Journal of Organic Evolution 47: 125-135.
2. Barrett, S. C. H., and C. G. Eckert. 1990. Variation and evolution of mating systems in seed plants. In S. Kawano [ed.], Biological approaches and evolutionary trends in plants, 229-254. Academic Press, London, UK.
3. Bassett, I. J., and D. B. Munro. 1986. The biology of Canadian weeds 78. Solanum carolinense L. and Solanum rostratum Dunal. Canadian Journal of Plant Science 66: 977-991.
4. Bello-Bedoy R and J Núñez-Farfán. 2010. Cost of inbreeding in resistance to herbivores in Datura stramonium. Annals of Botany 105: 747-753.
5. Bello-Bedoy R and J Núñez-Farfán. 2011. The effect of inbreeding on defense against multiple enemies in Datura stramonium. Journal of Evolutionary Biology 24: 518-530.
6. Berenbaum, M. R., and A. R. Zangerl. 2008. Facing the future of plant-insect interaction research: Le retour a la 'raison d'etre. Plant Physiology 146: 804-811.
7. Bergelson J and C. B. Purrington. 1996. Surveying patterns in the cost of resistance in plants. American Naturalist 148: 536-558.
8. Britton, N. L., and A B rown. 1970. An illustrated flora of the northeastern United States and Canada, vol. 1. Dover Publications, Mineola, New York, USA.
9. Carr, D. E., and M. D. Eubanks. 2002. Inbreeding alters resistance to insect herbivory and host plant quality in Mimulus guttatus (Scrophulariaceae). Evolution; International Journal of Organic Evolution 56: 22-30.
10. Charlesworth D and B Charlesworth. 1987. Inbreeding depression and its evolutionary consequences. Annual Review of Ecology and Systematics 18: 237-268.
11. Chien, J. C., and I. M. Sussex. 1996. Differential regulation of trichome formation on the adaxial and abaxial leaf surfaces by gibberellins and photoperiod in Arabidopsis thaliana (L.) Heynh. Plant Physiology 111: 1321-1328.
12. Cipollini, M. L., and D. J. Levey. 1997. Why are some fruits toxic? Glycoalkaloids in Solanum and fruit choice by vertebrates. Ecology 78: 782-798.
13. Cipollini M, L E Paulk and D F Cipollini. 2002. Effectofnitrogen and water treatment on leaf chemistry in horsenettle (Solanum caro-linense) and relationship to herbivory by flea beetles (Epitrix spp.) and tobacco hornworm (Manduca sexta). Journal of Chemical Ecology 28: 2377-2398.
14. Cooper, S. M., and T F Ginnett. 1998. Spines protect plants against browsing by small climbing mammals. Oecologia 113: 219-221.
15. Cooper, S. M., and N Owen-Smith. 1986. Effects of plant spinescence on large mammalian herbivores. Oecologia 68: 446-455.
16. De Moraes, C. M., W. J. Lewis, P. W. Paré, H T Alborn and J. H. Tumlinson. 1998. Herbivore-infested plants selectively attract para-sitoids. Nature 393: 570-573.
17. De Vos M and G Jander. 2009. Myzus persicae (green peach aphid) salivary components induce defence responses in Arabidopsis thaliana. Plant, Cell & Environment 32: 1548-1560.
18. Delphia C. M., J.R. Rohr, A G Stephenson, C. M. De Moraes and M C Mescher. 2009a. Effects of genetic variation and inbreeding on volatile production in a field population of horsenettle. International Journal of Plant Sciences 170: 12-20.
19. Delphia C. M., C. M. De Moraes, A. G. Stephenson and M. C. Mescher 2009b. Inbreeding in horsenettle influences herbivore resistance. Ecological Entomology 34: 513-519.
20. Dicke M and M W Sabelis. 1988. Infochemical terminology: Based on cost-benefit analysis rather than origin of compounds? Functional Ecology 2: 131-139.
21. Du D, JA Winsor, M Smith, A Denicco and A.G. Stephenson. 2008. Resistance and tolerance to herbivory changes with inbreeding and ontogeny in a wild gourd (Cucurbitaceae). American Journal of Botany 95: 84-92.
22. Duffey, S. S., and M. J. Stout. 1996. Antinutritive and toxic components of plant defense against insects. Archives of Insect Biochemistry and Physiology 32: 3-37.
23. Engelberth J H T, Alborn E., A. Schmelz and J. H. Tumlinson 2004. Airborne signals prime plants against insect herbivore attack. Proceedings of the National Academy of Sciences, USA 101: 1781-1785.
24. Gregory P., W. M. Tingey, D A Ave and P. Y. Bouthyette. 1986. Potato glandular trichomes: A physiochemical defense mechanism. In M. B. Green and P. A. Hedin [eds.], Natural resistance of plants to pests: Roles of allelochemicals, 160-167. American Chemical Society, Washington, D.C., USA.
25. Hare, J. D., E. Elle and N. M. Van Dam. 2003. Costs of glandular trichomes in Datura wrightii: A three year study. Evolution; International Journal of Organic Evolution 57: 793-805.
26. Hayes, C. N., J. A. Winsor and A. G. Stephenson. 2004. Inbreeding influences herbivory in Cucurbita pepo ssp. texana (Cucurbitaceae). Oecologia 140: 601-608.
27. Herms, D. A., and W J Mattson. 1992. The dilemma of plants: To grow or defend. The Quarterly Review of Biology 67: 283-335.
28. Hill, M. P., P. E. Hulley, J Allsopp and G Van Harmelen. 1997. Glandular trichomes on the exotic Solanum sisymbriifolium Lamarck (Solanaceae): Effective deterrents against an indigenous South African herbivore. African Entomology 5: 41-50.
29. Howe G. A., and G. Jander. 2008. Plant immunity to insect herbivores. Annual Review of Plant Biology 59: 41-66.
30. Hull-Sanders, H. M., and M. D. Eubanks. 2005. Plant defense theory provides insight into interactions involving inbred plants and insect herbivores. Ecology 86: 897-904.
31. Husband B. C., and D W Schemske. 1996. Evolution of the magnitude and timing of inbreeding depression in plants. Evolution; International Journal of Organic Evolution 50: 54-70.
32. Imura, O. 2003. Herbivorous arthropod community of an alien weed Solanum carolinense. Applied Entomology and Zoology 38: 293-300.
33. Karban R and J H Meyers. 1989. Induced responses to herbivory. Annual Review of Ecology and Systematics 20: 331-348.
34. Kariyat R. R., K. E. Mauck, C. M. De Moraes, A G Stephenson and M. C. M escher. 2012a. Inbreeding compromises volatile signaling phenotypes and influences tri-trophic interactions in horsenettle. Ecology Letters 15: 301-309.
35. Kariyat, R. R., J. M. Mena-Alí B Forry, M. C. Mescher, C. M. De Moraes and A. G. Stephenson. 2012b. Inbreeding, herbivory, and the transcriptome of Solanum carolinense L. Entomologia Experimentalis et Applicata 144: 134-144.
36. Kariyat, R. R., S. R. Scanlon, M. C. Mescher, C. M. De Moraes and A G. Stephenson. 2011. Inbreeding depression in Solanum carolinense (Solanaceae) under field conditions and implications for mating system evolution. PLoS ONE 6: e28459.
37. Kawagoe T K, K Shimizu, T Kakutani and H Kudoh. 2011. Coexistence of trichome variation in a natural plant population: A combined study using ecological and candidate gene approaches. PLoS ONE 6: E22184.
38. Kennedy, G. G. 2003. Tomato, pests, parasitoids, and predators: Tritrophic interactions involving the genus Lycopersicon. Annual Review of Entomology 48: 51-72.
39. Li G., Y. Yuan, Z. Lu, L. Yang, R. Gao, J. Lu, J. Li and G Xiong. 2012. Glabrous Rice 1, encoding a homeodomain protein, regulates trichome development in rice. Rice 5: 32.
40. Louda, S. M., M. A. Potvin and S. K. Collinge. 1990. Predispersal seed predation, postdispersal seed predation and competition in the recruitment of seedlings of a native thistle in sandhills prairie. American Midland Naturalist 124: 105-113.
41. McNaughton, S. J., D. A. Oesterheld, D. A. Frank and K J Williams 1989. Ecosystem level patterns of primary productivity and her-bivory of terrestrial ecosystems. Nature 341: 142-144.
42. Medeiros L and G. R. P. Moreira. 2002. Moving on hairy surfaces: Modifications of Gratiana spadicea larval legs to attach on its host plant Solanum sisymbriifolium. Entomologia Experimentalis et Applicata 102: 295-305.
43. Mena-alí, J. I. 2006. Dynamics of the self-incompatibility alleles in populations of Solanum carolinense. Ph.D. dissertation, State University, University Park, Pennsylvania, USA.
44. Mena-alí, J. I., L. H. Keiser and A. G. Stephenson. 2008. Inbreeding depression in Solanum carolinense (Solanaceae), a species with a plastic self-incompatibility response. BMC Evolutionary Biology 8: 10.
45. Mena-alí, J. I., and A. G. Stephenson. 2007. Segregation analyses of partial self-incompatibility in self and cross progeny of Solanum carolin-ense reveal a leaky S-allele. Genetics 177: 501-510.
46. Milewski A V, M Young and D Madden. 1991. Thorns as induced defenses: Experimental evidence. Oecologia 86: 70-75.
47. Neal, J. J., J. C. Steffens and W. M. Tingey. 1989. Glandular trichomes of Solanum berthaultii and resistance to the Colorado potato beetle. Entomologia Experimentalis et Applicata 51: 133-140.
48. Nykänen H and J Koricheva. 2004. Damage-induced changes in woody plants and their effects on insect herbivore performance: A meta-analysis. Oikos 104: 247-268.
49. Oliveira, P. S., V. Rico-Gray, C Diaz-Castelazo and C Castillo-Guevara. 1999. Interaction between ants, extrafloral nectaries, and insect herbivores in Neotropical coastal sand dunes: Herbivore deterrence by visiting ants increases fruit set in Opuntia stricta (Cactaceae). Functional Ecology 13: 623-631.
50. Peiffer, M., J. F. Tooker, D. S. Luthe and G. W. Felton. 2009. Plants on early alert: Glandular trichomes as sensors for insect herbivores. The New Phytologist 184: 644-656.
51. Purrington, C. B. 2000. Costs of resistance. Current Opinion in Plant Biology 3: 305-308.
52. Reymond P, N Bodenhausen, R. M. Van Poecke, V Krishnamurthy, M Dicke and E. E. Farmer. 2004. A conserved transcript pattern in response to a specialist and a generalist herbivore. The Plant Cell 16: 3132-3147.
53. Reymond, P., H. Weber, M Damond and E. E. Farmer. 2000. Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. The Plant Cell 12: 707-719.
54. Rhoades, D. F. 1979. Evolution of plant chemical defense against herbivores. In G. A. Rosenthal and D. H. Janzen [eds.], Herbivores: Their interaction with secondary plant metabolites, 3-54. Academic Press, New York, New York, USA.
55. Simms, E. L. 1992. Cost of plant resistance to herbivory. In R. S. Fritz and E. L. Simms [eds.], Plant resistance to herbivores and pathogens: Ecology, evolution, and genetics, 392-425. University of Chicago Press, Chicago, Illinois, USA.
56. Simms, E. L., and M. D. Rausher. 1987. Costs and benefits of plant resistance to herbivores. American Naturalist 130: 570-581.
57. Stephenson, A. G., B. Leyshon, S. E. Travers, C N Hayes and J. A. Winsor. 2004. Interrelationships among inbreeding, herbivory, and disease on reproduction in a wild gourd. Ecology 8 5: 3023-3034.
58. Travers, S. E., J. I. Menaalí and A. G. Stephenson. 2004. Plasticity in the self-incompatibility of Solanum carolinense. Plant Species Biology 19: 127-135.
59. Traw, M. B., and J Bergelson. 2003. Interactive effects of jasmonic acid salicylic acid and gibberellin on induction of trichomes in Arabidopsis. Plant Physiology 133: 1367-1375.
60. Weinig C L, A Dorn, N.C. Kane, M.C. Ungerer, S.S. Halldorsdottir, Z German, Y Toyonaga et al. 2003. Heterogeneous selection at specific loci in natural environments in Arabidopsis thaliana. Genetics 165: 321-329.
61. Wink, M. 2000. Interference of alkaloids with neuroreceptors and ion channels. In X. Atta-Ur-Rahman [ed.], Bioactive natural products, 3-129. Elsevier, Amsterdam, Netherlands.
62. Wise M. J. 2007a. The herbivores of Solanum carolinense (Horsenettle) in northern Virginia: Natural history and damage assessment. Southeastern Naturalist (Steuben, ME) 6: 505-522.
63. Wise, M. J. 2007b. Evolutionary ecology of resistance to herbivory: An investi gation of potential genetic constraints in the multiple-herbivore community of Solanum carolinense. The New Phytologist 175: 773-784.
64. Wise, M. J., and A. M. Weinberg. 2002. Prior flea beetle herbivory affects oviposition preference and larval performance of a potato beetle on their shared host plant. Ecological Entomology 2 7: 115-122.
65. Yencho, G. C., and W M Tingey. 1994. Glandular trichomes of Solanum berthaultii alter host preference of the Colorado potato beetle, Lepti-notarsa decemlineata. Entomologia Experimentalis et Applicata 70: 217-225.
66. Yoshida Y, R Sano, T Wada, J Takabayashi and K Okada 2009. Jasmonic acid control of GLABRA3 links inducible defense and trichome patterning in Arabidopsis. Development 136: 1039-1048.
67. Young, T. P., and A. P. Smith. 1994. Alpine herbivory on Mount Kenya. In P. W. Rundel, A. P. Smith, and F. C. Meinzer [eds.], Tropical alpine environments: Plant form and function, 219-235. Cambridge University Press, Cambridge, UK.
68. Young, T. P., M. L. Stanton and C. E. Christian. 2003. Effects of natural and simulated herbivory on spine lengths of Acacia drepanolobium in Kenya. Oikos 101: 171-179.
69. Yuan, J. S., T. G. Kolner, G Wiggins, G. J. Degenhardt et al. 2008. Molecular and genomic basis of volatile-mediated indirect defense against insects in rice. The Plant Journal 55: 491-503.