1932

Abstract

Costs of defense are central to our understanding of interactions between organisms and their environment, and defensive phenotypes of plants have long been considered to be constrained by trade-offs that reflect the allocation of limiting resources. Recent advances in uncovering signal transduction networks have revealed that defense trade-offs are often the result of regulatory “decisions” by the plant, enabling it to fine-tune its phenotype in response to diverse environmental challenges. We place these results in the context of classic studies in ecology and evolutionary biology, and propose a unifying framework for growth–defense trade-offs as a means to study the plant's allocation of limiting resources. Pervasive physiological costs constrain the upper limit to growth and defense traits, but the diversity of selective pressures on plants often favors negative correlations at intermediate trait levels. Despite the ubiquity of underlying costs of defense, the current challenge is using physiological and molecular approaches to predict the conditions where they manifest as detectable trade-offs.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-042916-040856
2017-04-28
2024-04-20
Loading full text...

Full text loading...

/deliver/fulltext/arplant/68/1/annurev-arplant-042916-040856.html?itemId=/content/journals/10.1146/annurev-arplant-042916-040856&mimeType=html&fmt=ahah

Literature Cited

  1. Agrawal AA.1.  2011. Current trends in the evolutionary ecology of plant defence. Funct. Ecol. 25:420–32 [Google Scholar]
  2. Agrawal AA, Hastings AP, Johnson MTJ, Maron JL, Salminen J-P. 2.  2012. Insect herbivores drive real-time ecological and evolutionary change in plant populations. Science 338:113–16 [Google Scholar]
  3. Agrawal AA, Kearney EE, Hastings AP, Ramsey TE. 3.  2012. Attenuation of the jasmonate burst, plant defensive traits, and resistance to specialist monarch caterpillars on shaded common milkweed (Asclepias syriaca). J. Chem. Ecol. 38:893–901 [Google Scholar]
  4. Agrawal AA, Strauss SY, Stout MJ. 4.  1999. Costs of induced responses and tolerance to herbivory in male and female fitness components of wild radish. Evolution 53:1093–104 [Google Scholar]
  5. Agrawal AA, Weber MG. 5.  2015. On the study of plant defence and herbivory using comparative approaches: How important are secondary plant compounds. Ecol. Lett. 18:985–91 [Google Scholar]
  6. Ågren J, Schemske DW. 6.  1993. The cost of defense against herbivores: an experimental study of trichome production in Brassica rapa. Am. Nat. 141:338–50 [Google Scholar]
  7. Almeida-Cortez JS, Shipley B, Arnason JT. 7.  1999. Do plant species with high relative growth rates have poorer chemical defences?. Funct. Ecol. 13:819–27 [Google Scholar]
  8. Arendt JD.8.  1997. Adaptive intrinsic growth rates: an integration across taxa. Q. Rev. Biol. 72:149–77 [Google Scholar]
  9. Arvidsson S, Pérez-Rodríguez P, Mueller-Roeber B. 9.  2011. A growth phenotyping pipeline for Arabidopsis thaliana integrating image analysis and rosette area modeling for robust quantification of genotype effects. New Phytol 191:895–907 [Google Scholar]
  10. Attaran E, Major IT, Cruz JA, Rosa BA, Koo AJK. 10.  et al. 2014. Temporal dynamics of growth and photosynthesis suppression in response to jasmonate signaling. Plant Physiol 165:1302–14 [Google Scholar]
  11. Babst BA, Ferrieri RA, Gray DW, Lerdau M, Schlyer DJ. 11.  et al. 2005. Jasmonic acid induces rapid changes in carbon transport and partitioning in Populus. New Phytol 167:63–72 [Google Scholar]
  12. Baldwin IT, Gorham D, Schmelz EA, Lewandowski CA, Lynds GY. 12.  1998. Allocation of nitrogen to an inducible defense and seed production in Nicotiana attenuata. Oecologia 115:541–52 [Google Scholar]
  13. Baldwin IT, Sims CL, Kean SE. 13.  1990. The reproductive consequences associated with inducible alkaloidal responses in wild tobacco. Ecology 71:252–62 [Google Scholar]
  14. Bekaert M, Edger PP, Hudson CM, Pires JC, Conant GC. 14.  2012. Metabolic and evolutionary costs of herbivory defense: systems biology of glucosinolate synthesis. New Phytol 196:596–605 [Google Scholar]
  15. Bergelson J.15.  1994. The effects of genotype and the environment on costs of resistance in lettuce. Am. Nat. 143:349–59 [Google Scholar]
  16. Bergelson J, Purrington CB. 16.  1996. Surveying patterns in the cost of resistance in plants. Am. Nat. 148:536–58 [Google Scholar]
  17. Brachi B, Meyer CG, Villoutreix R, Platt A, Morton TC. 17.  et al. 2015. Coselected genes determine adaptive variation in herbivore resistance throughout the native range of Arabidopsis thaliana. PNAS 112:4032–37 [Google Scholar]
  18. Burow M, Atwell S, Francisco M, Kerwin RE, Halkier BA, Kliebenstein DJ. 18.  2015. The glucosinolate biosynthetic gene AOP2 mediates feed-back regulation of jasmonic acid signaling in Arabidopsis. Mol. Plant 8:1201–12 [Google Scholar]
  19. Campos ML, Yoshida Y, Major IT, Ferreira DDO, Weraduwage SM. 19.  et al. 2016. Rewiring of jasmonate and phytochrome B signaling uncouples plant growth-defense tradeoffs. Nat. Commun. 7:12570 [Google Scholar]
  20. Carmona D, Fornoni J. 20.  2013. Herbivores can select for mixed defensive strategies in plants. New Phytol 197:576–85 [Google Scholar]
  21. Chen YH, Gols R, Benrey B. 21.  2015. Crop domestication and its impact on naturally selected trophic interactions. Annu. Rev. Entomol. 60:35–58 [Google Scholar]
  22. Cipollini D.22.  2002. Does competition magnify the fitness costs of induced responses in Arabidopsis thaliana? A manipulative approach. Oecologia 131:514–20 [Google Scholar]
  23. Cipollini D, Walters D, Voelckel C. 23.  2014. Costs of resistance in plants: from theory to evidence. Insect-Plant Interactions C Voelckel, G Jander 263–307 Annu. Plant Rev 47 Chichester, UK: Wiley & Sons [Google Scholar]
  24. Coley PD.24.  1988. Effects of plant growth rate and leaf lifetime on the amount and type of anti-herbivore defense. Oecologia 74:531–36 [Google Scholar]
  25. Coley PD, Bryant JP, Chapin FS. 25.  1985. Resource availability and plant antiherbivore defense. Science 230:895–99 [Google Scholar]
  26. Conner JK, Hartl DL. 26.  2004. A Primer of Ecological Genetics Sunderland, MA: Sinauer
  27. Corbineau F, Rudnicki RM, Come D. 27.  1988. The effects of methyl jasmonate on sunflower (Helianthus annuus L.) seed germination and seedling development. Plant Growth Regul 7:157–69 [Google Scholar]
  28. Cruz JA, Savage LJ, Zegarac R, Hall CC, Satoh-Cruz M. 28.  et al. 2016. Dynamic environmental photosynthetic imaging reveals emergent phenotypes. Cell Syst 2:365–77 [Google Scholar]
  29. Dathe W, Ronsch H, Preiss A, Schade W, Sembdner G, Schreiber K. 29.  1981. Endogenous plant hormones of the broad bean, Vicia faba L. (-)-jasmonic acid, a plant growth inhibitor in pericarp. Planta 153:530–35 [Google Scholar]
  30. de Wit M, Spoel SH, Sanchez-Perez GF, Gommers CMM, Pieterse CMJ. 30.  et al. 2013. Perception of low red:far-red ratio compromises both salicylic acid- and jasmonic acid-dependent pathogen defences in Arabidopsis. Plant J. 75:90–103 [Google Scholar]
  31. Denby KJ, Kumar P, Kliebenstein DJ. 31.  2004. Identification of Botrytis cinerea susceptibility loci in Arabidopsis thaliana. Plant J 38:473–86 [Google Scholar]
  32. Dobler S, Petschenka G, Pankoke H. 32.  2011. Coping with toxic plant compounds—the insect's perspective on iridoid glycosides and cardenolides. Phytochemistry 72:1593–604 [Google Scholar]
  33. Fakheran S, Paul-Victor C, Heichinger C, Schmid B, Grossniklaus U, Turnbull LA. 33.  2010. Adaptation and extinction in experimentally fragmented landscapes. PNAS 107:19120–25 [Google Scholar]
  34. Farmer EE.34.  2007. Plant biology: jasmonate perception machines. Nature 448:659–60 [Google Scholar]
  35. Feng SH, Martinez C, Gusmaroli G, Wang Y, Zhou JL. 35.  et al. 2008. Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature 451:475–79 [Google Scholar]
  36. Ferrieri AP, Agtuca B, Appel HM, Ferrieri RA, Schultz JC. 36.  2013. Temporal changes in allocation and partitioning of new carbon as 11C elicited by simulated herbivory suggest that roots shape aboveground responses in Arabidopsis. Plant Physiol. 161:692–704 [Google Scholar]
  37. Fine PVA, Miller ZJ, Mesones I, Irazuzta S, Appel HM. 37.  et al. 2006. The growth-defense trade-off and habitat specialization by plants in Amazonian forests. Ecology 87:S150–S62 [Google Scholar]
  38. Gershenzon J.38.  1994. The cost of plant chemical defense against herbivory: a biochemical perspective. Insect-Plant Interactions EA Bernays 105–73 Boca Raton, FL: CRC Press [Google Scholar]
  39. Gershenzon J.39.  1994. Metabolic costs of terpenoid accumulation in higher plants. J. Chem. Ecol. 20:1281–328 [Google Scholar]
  40. Giamoustaris A, Mithen R. 40.  1995. The effect of modifying the glucosinolate content of leaves of oilseed rape (Brassica napus ssp. oleifera) on its interaction with specialist and generalist pests. Ann. Appl. Biol 126:347–63 [Google Scholar]
  41. Gómez S, Ferrieri RA, Schueller M, Orians CM. 41.  2010. Methyl jasmonate elicits rapid changes in carbon and nitrogen dynamics in tomato. New Phytol 188:835–44 [Google Scholar]
  42. Halitschke R, Hamilton JG, Kessler A. 42.  2011. Herbivore-specific elicitation of photosynthesis by mirid bug salivary secretions in the wild tobacco Nicotiana attenuata. New Phytol. 191:528–35 [Google Scholar]
  43. Halkier BA, Gershenzon J. 43.  2006. Biology and biochemistry of glucosinolates. Annu. Rev. Plant Biol. 57:303–33 [Google Scholar]
  44. Hallik L, Niinemets U, Wright IJ. 44.  2009. Are species shade and drought tolerance reflected in leaf-level structural and functional differentiation in Northern Hemisphere temperate woody flora?. New Phytol 184:257–74 [Google Scholar]
  45. Harvell CD.45.  1990. The ecology and evolution of inducible defenses. Q. Rev. Biol. 65:323–40 [Google Scholar]
  46. Havko N, Major I, Jewell J, Attaran E, Browse J, Howe G. 46.  2016. Control of carbon assimilation and partitioning by jasmonate: an accounting of growth–defense tradeoffs. Plants 5:7 [Google Scholar]
  47. Heil M, Baldwin IT. 47.  2002. Fitness costs of induced resistance: emerging experimental support for a slippery concept. Trends Plant Sci 7:61–67 [Google Scholar]
  48. Heinrich M, Hettenhausen C, Lange T, Wunsche H, Fang JJ. 48.  et al. 2013. High levels of jasmonic acid antagonize the biosynthesis of gibberellins and inhibit the growth of Nicotiana attenuata stems. Plant J 73:591–606 [Google Scholar]
  49. Herms DA, Mattson WJ. 49.  1992. The dilemma of plants: to grow or defend. Q. Rev. Biol. 67:283–335 [Google Scholar]
  50. Howe GA.50.  2004. Jasmonates as signals in the wound response. J. Plant Growth Regul. 23:223–37 [Google Scholar]
  51. Huot B, Yao J, Montgomery BL, He SY. 51.  2014. Growth-defense tradeoffs in plants: a balancing act to optimize fitness. Mol. Plant 7:1267–87 [Google Scholar]
  52. Iwao K, Rausher MD. 52.  1997. Evolution of plant resistance to multiple herbivores: quantifying diffuse coevolution. Am. Nat. 149:316–35 [Google Scholar]
  53. Joseph B, Corwin JA, Züst T, Li B, Iravani M. 53.  et al. 2013. Hierarchical nuclear and cytoplasmic genetic architectures for plant growth and defense within Arabidopsis. Plant Cell 25:1929–45 [Google Scholar]
  54. Kakes P.54.  1989. An analysis of the costs and benefits of the cyanogenic system in Trifolium repens L. Theor. Appl. Genet. 77:111–18 [Google Scholar]
  55. Karban R, Baldwin IT. 55.  1997. Induced Responses to Herbivory Chicago: Univ. Chicago Press
  56. Katz E, Nisani S, Yadav BS, Woldemariam MG, Shai B. 56.  et al. 2015. The glucosinolate breakdown product indole-3-carbinol acts as an auxin antagonist in roots of Arabidopsis thaliana. Plant J. 82:547–55 [Google Scholar]
  57. Kempel A, Razanajatovo M, Stein C, Unsicker SB, Auge H. 57.  et al. 2015. Herbivore preference drives plant community composition. Ecology 96:2923–34 [Google Scholar]
  58. Kerwin R, Feusier J, Corwin J, Rubin M, Lin C. 58.  et al. 2015. Natural genetic variation in Arabidopsis thaliana defense metabolism genes modulates field fitness. eLife 4:e05604 [Google Scholar]
  59. Kessler D, Gase K, Baldwin IT. 59.  2008. Field experiments with transformed plants reveal the sense of floral scents. Science 321:1200–2 [Google Scholar]
  60. Kliebenstein DJ.60.  2016. False idolatry of the mythical growth versus immunity tradeoff in molecular systems plant pathology. Physiol. Mol. Plant Pathol. 95:55–59 [Google Scholar]
  61. Kloth KJ, Wiegers GL, Busscher-Lange J, van Haarst JC, Kruijer W. 61.  et al. 2016. AtWRKY22 promotes susceptibility to aphids and modulates salicylic acid and jasmonic acid signalling. J. Exp. Bot. 67:3383–96 [Google Scholar]
  62. Koornneef A, Pieterse CMJ. 62.  2008. Cross talk in defense signaling. Plant Physiol 146:839–44 [Google Scholar]
  63. Koricheva J.63.  2002. Meta-analysis of sources of variation in fitness costs of plant antiherbivore defenses. Ecology 83:176–90 [Google Scholar]
  64. Kroes A, van Loon JJA, Dicke M. 64.  2015. Density-dependent interference of aphids with caterpillar-induced defenses in Arabidopsis: involvement of phytohormones and transcription factors. Plant Cell Physiol 56:98–106 [Google Scholar]
  65. Kunkel BN, Brooks DM. 65.  2002. Cross talk between signaling pathways in pathogen defense. Curr. Opin. Plant Biol. 5:325–31 [Google Scholar]
  66. Leone M, Keller MM, Cerrudo I, Ballaré CL. 66.  2014. To grow or defend? Low red:far-red ratios reduce jasmonate sensitivity in Arabidopsis seedlings by promoting DELLA degradation and increasing JAZ10 stability. New Phytol. 204:355–67 [Google Scholar]
  67. Li J, Brader G, Kariola T, Palva ET. 67.  2006. WRKY70 modulates the selection of signaling pathways in plant defense. Plant J 46:477–91 [Google Scholar]
  68. Li J, Brader G, Palva ET. 68.  2004. The WRKY70 transcription factor: a node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defense. Plant Cell 16:319–31 [Google Scholar]
  69. Li R, Zhang J, Li J, Zhou G, Wang Q. 69.  et al. 2015. Prioritizing plant defence over growth through WRKY regulation facilitates infestation by non-target herbivores. eLife 4:e04805 [Google Scholar]
  70. Li X, Schmid B, Wang F, Paine CET. 70.  2016. Net assimilation rate determines the growth rates of 14 species of subtropical forest trees. PLOS ONE 11:e0150644 [Google Scholar]
  71. Lind EM, Borer E, Seabloom E, Adler P, Bakker JD. 71.  et al. 2013. Life-history constraints in grassland plant species: a growth-defence trade-off is the norm. Ecol. Lett. 16:513–21 [Google Scholar]
  72. Loranger J, Meyer ST, Shipley B, Kattge J, Loranger H. 72.  et al. 2012. Predicting invertebrate herbivory from plant traits: evidence from 51 grassland species in experimental monocultures. Ecology 93:2674–82 [Google Scholar]
  73. Lozano-Duran R, Zipfel C. 73.  2015. Trade-off between growth and immunity: role of brassinosteroids. Trends Plant Sci 20:12–19 [Google Scholar]
  74. Machado RAR, Ferrieri AP, Robert CAM, Glauser G, Kallenbach M, Baldwin IT. 74.  2013. Leaf-herbivore attack reduces carbon reserves and regrowth from the roots via jasmonate and auxin signaling. New Phytol. 200:1234–46 [Google Scholar]
  75. Machado RAR, McClure M, Hervé MR, Baldwin IT, Erb M. 75.  2016. Benefits of jasmonate-dependent defenses against vertebrate herbivores in nature. eLife 5:e13720 [Google Scholar]
  76. Marak HB, Biere A, Van Damme JMM. 76.  2003. Fitness costs of chemical defense in Plantago lanceolata L.: effects of nutrient and competition stress. Evolution 57:2519–30 [Google Scholar]
  77. Mason CM, Bowsher AW, Crowell BL, Celoy RM, Tsai C-J, Donovan LA. 77.  2016. Macroevolution of leaf defenses and secondary metabolites across the genus Helianthus. New Phytol. 209:1720–33 [Google Scholar]
  78. Mauricio R, Rausher MD. 78.  1997. Experimental manipulation of putative selective agents provides evidence for the role of natural enemies in the evolution of plant defense. Evolution 51:1435–44 [Google Scholar]
  79. Meldau S, Ullman-Zeunert L, Govind G, Bartram S, Baldwin IT. 79.  2012. MAPK-dependent JA and SA signalling in Nicotiana attenuata affects plant growth and fitness during competition with conspecifics. BMC Plant Biol 12:213 [Google Scholar]
  80. Moles AT, Peco B, Wallis IR, Foley WJ, Poore AGB. 80.  et al. 2013. Correlations between physical and chemical defences in plants: tradeoffs, syndromes, or just many different ways to skin a herbivorous cat?. New Phytol 198:252–63 [Google Scholar]
  81. Munch SB, Conover DO. 81.  2004. Nonlinear cost in Menidia menidia: theory and empirical evidence. Evolution 58:661–64 [Google Scholar]
  82. Nardini A, Peda G, La Rocca N. 82.  2012. Trade-offs between leaf hydraulic capacity and drought vulnerability: morpho-anatomical bases, carbon costs and ecological consequences. New Phytol 196:788–98 [Google Scholar]
  83. Navarro L, Bari R, Achard P, Lison P, Nemri A. 83.  et al. 2008. DELLAs control plant immune responses by modulating the balance and salicylic acid signaling. Curr. Biol. 18:650–55 [Google Scholar]
  84. Onkokesung N, Reichelt M, van Doorn A, Schuurink RC, Dicke M. 84.  2016. Differential costs of two distinct resistance mechanisms induced by different herbivore species in Arabidopsis. Plant Physiol. 170:891–906 [Google Scholar]
  85. Paine CET, Marthews TR, Vogt DR, Purves D, Rees M. 85.  et al. 2012. How to fit nonlinear plant growth models and calculate growth rates: an update for ecologists. Methods Ecol. Evol. 3:245–56 [Google Scholar]
  86. Paschold A, Halitschke R, Baldwin IT. 86.  2007. Co(i)-ordinating defenses: NaCOI1 mediates herbivore-induced resistance in Nicotiana attenuata and reveals the role of herbivore movement in avoiding defenses. Plant J 51:79–91 [Google Scholar]
  87. Paul-Victor C, Turnbull LA. 87.  2009. The effect of growth conditions on the seed size/number trade-off. PLOS ONE 4:e6917 [Google Scholar]
  88. Paul-Victor C, Züst T, Rees M, Kliebenstein DJ, Turnbull LA. 88.  2010. A new method for measuring relative growth rate can uncover the costs of defensive compounds in Arabidopsis thaliana. New Phytol. 187:1102–11 [Google Scholar]
  89. Pearse IS, Hipp AL. 89.  2012. Global patterns of leaf defenses in oak species. Evolution 66:2272–86 [Google Scholar]
  90. Pellissier L, Litsios G, Fishbein M, Salamin N, Agrawal AA, Rasmann S. 90.  2016. Different rates of defense evolution and niche preferences in clonal and nonclonal milkweeds (Asclepias spp.). New Phytol 209:1230–39 [Google Scholar]
  91. Pilson D.91.  2000. The evolution of plant response to herbivory: simultaneously considering resistance and tolerance in Brassica rapa. Evol. Ecol. 14:457–89 [Google Scholar]
  92. Prasad KVSK, Song B-H, Olson-Manning C, Anderson JT, Lee C-R. 92.  et al. 2012. A gain-of-function polymorphism controlling complex traits and fitness in nature. Science 337:1081–84 [Google Scholar]
  93. Rausher MD, Simms EL. 93.  1989. The evolution of resistance to herbivory in Ipomoea purpurea. 1. Attempts to detect selection. Evolution 43:563–72 [Google Scholar]
  94. Redman AM, Cipollini DF, Schultz JC. 94.  2001. Fitness costs of jasmonic acid-induced defense in tomato, Lycopersicon esculentum. Oecologia 126:380–85 [Google Scholar]
  95. Rees M, Osborne CP, Woodward FI, Hulme SP, Turnbull LA, Taylor SH. 95.  2010. Partitioning the components of relative growth rate: How important is plant size variation?. Am. Nat. 176:E152–61 [Google Scholar]
  96. Reich PB, Walters MB, Ellsworth DS. 96.  1997. From tropics to tundra: global convergence in plant functioning. PNAS 94:13730–34 [Google Scholar]
  97. Robert CAM, Ferrieri RA, Schirmer S, Babst BA, Schueller MJ. 97.  et al. 2014. Induced carbon reallocation and compensatory growth as root herbivore tolerance mechanisms. Plant Cell Environ 37:2613–22 [Google Scholar]
  98. Rose KE, Atkinson RL, Turnbull LA, Rees M. 98.  2009. The costs and benefits of fast living. Ecol. Lett. 12:1379–84 [Google Scholar]
  99. Schwachtje J, Minchin PEH, Jahnke S, van Dongen JT, Schittko U, Baldwin IT. 99.  2006. SNF1-related kinases allow plants to tolerate herbivory by allocating carbon to roots. PNAS 103:12935–40 [Google Scholar]
  100. Siemens DH, Mitchell-Olds T. 100.  1996. Glucosinolates and herbivory by specialists (Coleoptera: Chrysomelidae, Lepidoptera: Plutellidae): consequences of concentration and induced resistance. Environ. Entomol. 25:1344–53 [Google Scholar]
  101. Siemens DH, Mitchell-Olds T. 101.  1998. Evolution of pest-induced defenses in Brassica plants: tests of theory. Ecology 79:632–46 [Google Scholar]
  102. Simms EL.102.  1992. Costs of plant resistance to herbivory. Plant Resistance to Herbivores and Pathogens: Ecology, Evolution and Genetics RS Fritz, EL Simms 392–425 Chicago: Univ. Chicago Press [Google Scholar]
  103. Simms EL, Rausher MD. 103.  1987. Costs and benefits of plant resistance to herbivory. Am. Nat. 130:570–81 [Google Scholar]
  104. Stanton MA, Ullmann-Zeunert L, Wielsch N, Bartram S, Svatos A. 104.  et al. 2013. Silencing ribulose-1,5-bisphosphate carboxylase/oxygenase expression does not disrupt nitrogen allocation to defense after simulated herbivory in Nicotiana attenuata. Plant Signal. Behav. 8:e27570 [Google Scholar]
  105. Staswick PE, Tiryaki I. 105.  2004. The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis. Plant Cell 16:2117–27 [Google Scholar]
  106. Steppuhn A, Gase K, Krock B, Halitschke R, Baldwin IT. 106.  2004. Nicotine's defensive function in nature. PLOS Biol 2:1074–80 [Google Scholar]
  107. Stowe KA.107.  1998. Experimental evolution of resistance in Brassica rapa: correlated response of tolerance in lines selected for glucosinolate content. Evolution 52:703–12 [Google Scholar]
  108. Stowe KA, Marquis RJ. 108.  2011. Costs of defense: correlated responses to divergent selection for foliar glucosinolate content in Brassica rapa. Evol. Ecol. 25:763–75 [Google Scholar]
  109. Strauss SY, Siemens DH, Decher MB, Mitchell-Olds T. 109.  1999. Ecological costs of plant resistance to herbivores in the currency of pollination. Evolution 53:1105–13 [Google Scholar]
  110. Sun TP.110.  2011. The molecular mechanism and evolution of the GA-GID1-DELLA signaling module in plants. Curr. Biol. 21:R338–R45 [Google Scholar]
  111. Thaler JS, Humphrey PT, Whiteman NK. 111.  2012. Evolution of jasmonate and salicylate signal crosstalk. Trends Plant Sci 17:260–70 [Google Scholar]
  112. Tiffin P, Rausher MD. 112.  1999. Genetic constraints and selection acting on tolerance to herbivory in the common morning glory Ipomoea purpurea. Am. Nat. 154:700–16 [Google Scholar]
  113. Todesco M, Balasubramanian S, Hu TT, Traw MB, Horton M. 113.  et al. 2010. Natural allelic variation underlying a major fitness trade-off in Arabidopsis thaliana. Nature 465:632–36 [Google Scholar]
  114. Turnbull LA, Paul-Victor C, Schmid B, Purves DW. 114.  2008. Growth rates, seed size, and physiology: Do small-seeded species really grow faster?. Ecology 89:1352–63 [Google Scholar]
  115. Turnbull LA, Philipson CD, Purves DW, Atkinson RL, Cunniff J. 115.  et al. 2012. Plant growth rates and seed size: a re-evaluation. Ecology 93:1283–89 [Google Scholar]
  116. Ueda J, Kato J. 116.  1982. Inhibition of cytokinin-induced plant-growth by jasmonic acid and its methyl-ester. Physiol. Plant. 54:249–52 [Google Scholar]
  117. Van Dam NM, Baldwin IT. 117.  2001. Competition mediates costs of jasmonate-induced defences, nitrogen acquisition and transgenerational plasticity in Nicotiana attenuata. Funct. Ecol. 15:406–15 [Google Scholar]
  118. Van Dam NM, Baldwin IT. 118.  2003. Heritability of a quantitative and qualitative protease inhibitor polymorphism in Nicotiana attenuata. Plant Biol 5:179–85 [Google Scholar]
  119. Walling LL.119.  2000. The myriad plant responses to herbivores. J. Plant Growth Regul. 19:195–216 [Google Scholar]
  120. Wang L, Allmann S, Wu JS, Baldwin IT. 120.  2008. Comparisons of LIPOXYGENASE3- and JASMONATE-RESISTANT4/6-silenced plants reveal that jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore resistance of Nicotiana attenuata. Plant Physiol. 146:904–15 [Google Scholar]
  121. Wang WF, Wang ZY. 121.  2014. At the intersection of plant growth and immunity. Cell Host Microbe 15:401–3 [Google Scholar]
  122. White AC, Rogers A, Rees M, Osborne CP. 122.  2015. How can we make plants grow faster? A source–sink perspective on growth rate. J. Exp. Bot. 67:31–45 [Google Scholar]
  123. Whittaker RH, Feeny PP. 123.  1971. Allelochemics: chemical interactions between species. Science 171:757–70 [Google Scholar]
  124. Wise MJ, Rausher MD. 124.  2016. Costs of resistance and correlational selection in the multiple-herbivore community of Solanum carolinense. Evolution 70:2411–20 [Google Scholar]
  125. Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z. 125.  et al. 2004. The worldwide leaf economics spectrum. Nature 428:821–27 [Google Scholar]
  126. Wu J, Baldwin IT. 126.  2010. New insights into plant responses to the attack from insect herbivores. Annu. Rev. Genet. 44:1–24 [Google Scholar]
  127. Wu J, Hettenhausen C, Meldau S, Baldwin IT. 127.  2007. Herbivory rapidly activates MAPK signaling in attacked and unattacked leaf regions but not between leaves of Nicotiana attenuata. Plant Cell 19:1096–122 [Google Scholar]
  128. Yang DL, Yao J, Mei CS, Tong XH, Zeng LJ. 128.  et al. 2012. Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade. PNAS 109:E1192–200 [Google Scholar]
  129. Zangerl AR, Berenbaum MR. 129.  1997. Cost of chemically defending seeds: furanocoumarins and Pastinaca sativa. Am. Nat. 150:491–504 [Google Scholar]
  130. Zavala JA, Patankar AG, Gase K, Baldwin IT. 130.  2004. Constitutive and inducible trypsin proteinase inhibitor production incurs large fitness costs in Nicotiana attenuata. PNAS 101:1607–12 [Google Scholar]
  131. Zhang J, Peng YL, Guo ZJ. 131.  2008. Constitutive expression of pathogen-inducible OsWRKY31 enhances disease resistance and affects root growth and auxin response in transgenic rice plants. Cell Res 18:508–21 [Google Scholar]
  132. Zhang SQ, Klessig DF. 132.  2001. MAPK cascades in plant defense signaling. Trends Plant Sci 6:520–27 [Google Scholar]
  133. Zhang Y, Turner JG. 133.  2008. Wound-induced endogenous jasmonates stunt plant growth by inhibiting mitosis. PLOS ONE 3:e3699 [Google Scholar]
  134. Zhou GX, Qi JF, Ren N, Cheng JA, Erb M. 134.  et al. 2009. Silencing OsHI-LOX makes rice more susceptible to chewing herbivores, but enhances resistance to a phloem feeder. Plant J 60:638–48 [Google Scholar]
  135. Züst T, Heichinger C, Grossniklaus U, Harrington R, Kliebenstein DJ, Turnbull LA. 135.  2012. Natural enemies drive geographic variation in plant defenses. Science 338:116–19 [Google Scholar]
  136. Züst T, Joseph B, Shimizu KK, Kliebenstein DJ, Turnbull LA. 136.  2011. Using knockout mutants to reveal the costs of defensive traits. Proc. R. Soc. B 278:2598–603 [Google Scholar]
  137. Züst T, Rasmann S, Agrawal AA. 137.  2015. Growth-defense tradeoffs for two major anti-herbivore traits of the common milkweed Asclepias syriaca. Oikos 124:1404–15 [Google Scholar]
/content/journals/10.1146/annurev-arplant-042916-040856
Loading
/content/journals/10.1146/annurev-arplant-042916-040856
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error