Abstract
Key message
Chemical defenses are imperative for plant survival, but their production is often associated with growth restrictions. Here we review the most recent theories to explain this complex dilemma of plants.
Abstract
Plants are a nutritional source for a myriad of pests and pathogens that depend on green tissues to complete their life cycle. Rather than remaining passive victims, plants utilize an arsenal of chemical defenses to fend off biotic attack. While the deployment of such barriers is imperative for survival, the production of these chemical defenses is typically associated with negative impacts on plant growth. Here we discuss the most recent theories which explain this highly dynamic growth versus defense dilemma. Firstly, we discuss the hypothesis that the antagonism between the accumulation of chemical defenses and growth is rooted in the evolutionary history of plants and may be a consequence of terrestrialization. Then, we revise the different paradigms available to explain the growth versus chemical defense antagonism, including recent findings that update these into more comprehensive and plausible theories. Finally, we highlight state-of-the-art strategies that are now allowing the activation of growth and the concomitant production of chemical barriers in plants. Growth versus chemical defense antagonism imposes large ecological and economic costs, including increased crop susceptibility to pests and pathogens. In a world where these plant enemies are the main problem to increase food production, we believe that this review will summarize valuable information for future studies aiming to breed highly defensive plants without the typical accompanying penalties to growth.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Agrawal AA, Hastings AP, Johnson MTJ, Maron JL, Salminen JP (2012) Insect herbivores drive real-time ecological and evolutionary changes in plant populations. Science 338:113–116. https://doi.org/10.1126/science.1225977
Aharoni A, Galili G (2011) Metabolic engineering of the plant primary-secondary metabolism interface. Curr Opin Biotechnol 22:239–244. https://doi.org/10.1016/j.copbio.2010.11.004
Attaran E, Major IT, Cruz JA, Rosa BA, Koo AJK, Chen J, Kramer DM, He SY, Howe GA (2014) Temporal dynamics of growth and photosynthesis suppression in response to jasmonate signaling. Plant Phys 165:1302–1314. https://doi.org/10.1104/pp.114.239004
Baldwin IT, Callahan P (1993) Autotoxicity and chemical defense: nicotine accumulation and carbon gain in solanaceous plants. Oecologia 94:534–541. https://doi.org/10.1007/BF00566969
Ballaré CL, Austin AT (2019) Recalculating growth and defense strategies under competition: key roles of photoreceptors and jasmonates. J Exp Bot 70:3425–3434. https://doi.org/10.1093/jxb/erz237
Ballhorn D (2011) Constraints of simultaneous resistance to a fungal pathogen and an insect herbivore in lima bean (Phaseolus lunatus L.). J Chem Ecol 37:141–144. https://doi.org/10.1007/s10886-010-9905-0
Bally J, Nakasugi K, Jia F, Jung H, Ho SYW, Wong M, Paul CM, Naim F, Wood CC, Crowhurst RN et al (2015) The extremophile Nicotiana benthamiana has traded viral defence for early vigor. Nat Plants 1:15165. https://doi.org/10.1038/nplants.2015.165
Bastias DA, Gianoli E, Gundel PE (2021) Fungal endophytes can eliminate the plant growth-defence trade-off. New Phytol 230:2105–2113. https://doi.org/10.1111/nph.17335
Bastias DA, Martínez-Ghersa MA, Ballaré CL, Gundel PE (2017) Epichloë fungal endophytes and plant defenses: not just alkaloids. Trends Plant Sci 22:939–948. https://doi.org/10.1016/j.tplants.2017.08.005
Bastias DA, Martínez-Ghersa MA, Newman JA, Card SD, Mace WJ, Gundel PE (2018) The plant hormone salicylic acid interacts with the mechanism of anti-herbivory conferred by fungal endophytes in grasses. Plant Cell Environ 41:395–405. https://doi.org/10.1111/pce.13102
Baggs EL, Monroe JG, Thanki AS, O’Grady R, Schudoma C, Haerty W, Krasileva KV (2020) Convergent loss of an EDS1/PAD4 signaling pathway in several plant lineages reveals coevolved components of plant immunity and drought response. Plant Cell 32:2158–2177. https://doi.org/10.1105/tpc.19.00903
Baracchi D, Marples A, Jenkins AJ, Leitch AR, Chittka L (2017) Nicotine in floral nectar pharmacologically influences bumblebee learning of floral features. Sci Rep 7:1951. https://doi.org/10.1038/s41598-017-01980-1
Besseau S, Hoffmann L, Geoffroy P, Lapierre C, Pollet B, Legrand M (2007) Flavonoid accumulation in Arabidopsis repressed in lignin synthesis affects auxin transport and plant growth. Plant Cell 19:148–162. https://doi.org/10.1105/tpc.106.044495
Bekaert M, Edger PP, Hudson CM, Pires JC, Conant GC (2012) Metabolic and evolutionary costs of herbivory defense: systems biology of glucosinolate synthesis. New Phytol 196:596–605. https://doi.org/10.1111/j.1469-8137.2012.04302.x
Berens ML, Berry HM, Mine A, Argueso CT, Tsuda K (2017) Evolution of hormone signaling networks in plant defense. Annu Rev Phytopatol 55:401–425. https://doi.org/10.1146/annurev-phyto-080516-035544
Bowman JL, Kohchi T, Yamato KT, Jenkins J, Shu S, Ishizaki K, Yamaoka S, Nishihama R, Nakamura Y, Berger F et al (2017) Insights into land plant evolution garnered from the Marchantia polymorpha genome. Cell 171:287–304. https://doi.org/10.1016/j.cell.2017.09.030
Campos ML, Almeida M, Rossi ML, Martinelli AP, Litholdo Junior CG, Figueira A, Rampelotti-Ferreira FT, Vendramim JD, Benedito VA, Peres LEP (2009) Brassinosteroids interact negatively with jasmonates in the formation of anti-herbivory traits in tomato. J Exp Bot 60:4347–4361. https://doi.org/10.1093/jxb/erp270
Campos ML, Kang JL, Howe GA (2014) Jasmonate-triggered plant immunity. J Chem Ecol 40:657–675. https://doi.org/10.1007/s10886-014-0468-3
Campos ML, Yoshida Y, Major IT, Ferreira DO, Weraduwage SM, Froehlich JE, Johnson BF, Kramer DM, Jander G, Sharkey TD, Howe GA (2016) Rewiring of jasmonate and phytochrome B signalling uncouples plant growth-defense tradeoffs. Nat Commun 7:12570. https://doi.org/10.1038/ncomms12570
Campos ML, Souza CM, Oliveira KBS, Dias SC, Franco OL (2018) The role of antimicrobial peptides in plant immunity. J Exp Bot 69:4997–5011. https://doi.org/10.1093/jxb/ery294
Cerrudo I, Caliri-Ortiz E, Keller MM, Degano E, Demkura PV, Ballaré CL (2017) Exploring growth-defence trade-offs in Arabidopsis: phytochrome B inactivation requires JAZ10 to suppress plant immunity but not to trigger shade-avoidance responses. Plant Cell Environ 40:635–644. https://doi.org/10.1111/pce.12877
Chen YD, Moles A, Bu ZJ, Zhang MM, Wang ZC, Zhao HY (2021) Induced defense and its costs in two bryophyte species. Am J Bot 108:777–787. https://doi.org/10.1002/ajb2.1654
Christensen SA, Sims J, Vaughan MM, Hunter C, Block A, Willett D, Alborn HT, Huffaker A, Schmelz EA (2018) Commercial hybrids and mutant genotypes reveal complex protective roles for inducible terpenoid defenses in maize. J Exp Bot 69:1693–1705. https://doi.org/10.1093/jxb/erx495
Cipollini D, Walters D, Voelckel C (2014) Costs of resistance in plants: From theory to evidence. In: Roberts JA (ed) Annual Plant Reviews. Wiley, Hoboken, NJ, pp 263–307. https://doi.org/10.1002/9781118829783.ch8
Cope OL, Keefover-Ring K, Kruger EL, Lindroth RL (2021) Growth-defense trade-offs shape population genetic composition in an iconic forest tree species. Proc Nat Acad Sci USA 118:e2103162118. https://doi.org/10.1073/pnas.2103162118
De Bruyne L, Hofte M, De Vleesschauwer D (2014) Connecting growth and defense: the emerging role of brassinosteroids and gibberellins in plant innate immunity. Mol Plant 7:943–959. https://doi.org/10.1093/mp/ssu050
de Vries J, Archibald JM (2018) Plant evolution: landmarks on the path to terrestrial life. New Phyol 217:1428–1434. https://doi.org/10.1111/nph.14975
de Vries J, Curtis BA, Gould SB, Archibald JM (2018) Embryophyte stress signaling evolved in the algal progenitors of land plants. Proc Natl Acad Sci USA 115:E3471–E3840. https://doi.org/10.1073/pnas.1719230115
Delaux PM, Nanda AK, Mathé C, Sejalon-Delmas N, Dunand C (2012) Molecular and biochemical aspects of plant terrestrialization. Perspect Plant Ecol 14:49–59. https://doi.org/10.1016/j.ppees.2011.09.001
Dong X, Gao Y, Chen W, Wang W, Gong L, Liu X, Luo J (2015) Spatiotemporal distribution of phenolamides and the genetics of natural variation of hydroxycinnamoyl spermidine in rice. Mol Plant 8:111–121. https://doi.org/10.1016/j.molp.2014.11.003
Dupond PY, Eaton CJ, Wargent JJ, Fechtner S, Solomon P, Schmid J, Day RC, Scott B, Cox MP (2015) Fungal endophyte infection of ryegrass reprograms host metabolism and alters development. New Phytol 208:1227–1240. https://doi.org/10.1111/nph.13614
Erb M, Kliebenstein DJ (2020) Plant secondary metabolites as defenses, regulators, and primary metabolites: The blurred functional trichotomy. Plant Phys 184:39–52. https://doi.org/10.1104/pp.20.00433
Fang C, Fernie AR, Luo J (2019) Exploring the diversity of plant metabolism. Trends Plant Sci 24:83–98. https://doi.org/10.1016/j.tplants.2018.09.006
Farias RP, Costa LEN, Oliveira AFM, Barros ICL, Mehltreter K (2020) Leaf defense syndromes in tropical ferns. Plant Ecol 221:853–865. https://doi.org/10.1007/s11258-019-00983-4
Fernandez C, Monnier Y, Santonja M, Gallet C, Weston LA, Prévosto B, Saunier A, Baldy V, Bousquet-Mélou A (2016) The impact of competition and allelopathy on the trade-off between plant defense and growth in two contrasting tree species. Front Plant Sci 7:594. https://doi.org/10.3389/fpls.2016.00594
Field B, Osbourn AE (2008) Metabolic diversification – independent assembly of operon-like gene clusters in different plants. Science 320:543–547. https://doi.org/10.1126/science.1154990
Field B, Fiston-Lavier AS, Kemen A, Geisler K, Quesneville H, Osbourn AE (2011) Formation of plant metabolic gene clusters within dynamic chromosomal regions. Proc Natl Acad Sci USA 108:16116–16121. https://doi.org/10.1073/pnas.1109273108
Figueroa-Macías JP, García YC, Núñez M, Díaz K, Olea AF, Espinoza L (2021) Plant growth-defense trade-offs: molecular processes leading to physiological changes. Int J Mol Sci 22:693. https://doi.org/10.3390/ijms22020693
Fine PVA, Miller ZJ, Mesones I, Irazuzta S, Appel HM, Stevens HH, Saaksjarvi I, Schultz JC, Coley PD (2006) The growth-defense trade-off and habitat specialization by plants in amazonian forests. Ecology 87:S150–S162. https://doi.org/10.1890/0012-9658(2006)87[150:TGTAHS]2.0.CO;2
Foyer CH, Noctor G, Emden HFV (2007) An evaluation of the costs of making specific secondary metabolites: does the yield penalty incurred by host plant resistance to insects result from competition for resources? Int J Pest Manag 53:175–183. https://doi.org/10.1080/09670870701469146
Frailie TB, Innes RW (2021) Engineering healthy crops: molecular strategies for enhancing the plant immune system. Curr Opin Biotechnol 70:151–157. https://doi.org/10.1016/j.copbio.2021.04.006
Frost CJ, Mescher MC, Carlson JE, Moraes CM (2008) Plant defense priming against herbivores: getting ready for a different battle. Plant Physiol 146:818–824. https://doi.org/10.1104/pp.107.113027
Gao Y, Wang W, Zhang T, Gong Z, Zhao H, Han GZ (2018) Out of water: the origin and early diversification of plant R-genes. Plant Physiol 177:82–89. https://doi.org/10.1104/pp.18.00185
Garcia A, Martinez M, Diaz I, Santa-Maria ME (2021) The price of the induced defense against pests: a meta-analysis. Front Plant Sci 11:615122. https://doi.org/10.3389/fpls.2020.615122
Gasparini K, Moreira JR, Peres LEP, Zsogon A (2021) De novo domestication of wild species to create crops with increased resilience and nutritional value. Curr Opin Plant Biol 60:102006. https://doi.org/10.1016/j.pbi.2021.102006
Gershenzon J (1994) Metabolic costs of terpenoid accumulation in higher plants. J Chem Ecol 20:1281–1328. https://doi.org/10.1007/BF02059810
Gianoli E (2002) A phenotypic trade-off between constitutive defenses and induced responses in wheat seedlings. Ecoscience 9:482–488. https://doi.org/10.1080/11956860.2002.11682736
Gommers CMM, Keuskamp DH, Buti S, Veen H, Koevoets IT, Reinen E, Voesenek LACJ, Pierik R (2017) Molecular profiles of contrasting shade response strategies in wild plants: differential control of immunity and shoot elongation. Plant Cell 29:331–344. https://doi.org/10.1105/tpc.16.00790
Guo Q, Major IT, Howe GA (2018a) Resolution of growth-defense conflict: mechanistic insights from jasmonate signaling. Curr Opin Plant Biol 44:72–81. https://doi.org/10.1016/j.pbi.2018.02.009
Guo Q, Yoshida Y, Major IT, Wang K, Sugimoto K, Kapali G, Havko NE, Benning C, Howe GA (2018b) JAZ repressors of metabolic defense promote growth and reproductive fitness in Arabidopsis. Proc Natl Acad Sci USA 115:E10768–E10777. https://doi.org/10.1073/pnas.1811828115
Ha CM, Rao X, Saxena G, Dixon RA (2021) Growth-defense trade-offs and yield loss in plants with engineered cell walls. New Phytol 231:60–74. https://doi.org/10.1111/nph.17383
Haak DC, McGinnis LA, Levey DJ, Tewksbury JJ (2012) Why are not all chilies hot? A trade-off limits pungency. Proc R Soc B. https://doi.org/10.1098/rspb.2011.2091. 279:2012-2017
Han GZ (2019) Origin and evolution of the plant immune system. New Phytol 222:70–83. https://doi.org/10.1111/nph.15596
Hartmann T (2007) From waste products to ecochemicals: Fifty years research of plant secondary metabolism. Phytochemistry 68:2831–2846. https://doi.org/10.1016/j.phytochem.2007.09.017
Havko NE, Major IT, Jewell JB, Attaran E, Browse J, Howe GA (2016) Control of carbon assimilation and partitioning by jasmonate: an accounting of growth-defense tradeoffs. Plants 5:7. https://doi.org/10.3390/plants5010007
Hay ME (1991) Marine-terrestrial contrasts in the ecology of plant chemical defenses against herbivores. Trees 6:362–365. https://doi.org/10.1016/0169-5347(91)90227-O
Hayashi S, Watanabe M, Kobayashi M, Tohge T, Hashimoto T, Shoji T (2020) Genetic manipulation of transcriptional regulators alters nicotine biosynthesis in tobacco. Plant Cell Physiol 61:1041–1053. https://doi.org/10.1093/pcp/pcaa036
Heil M, Baldwin IT (2002) Fitness costs of induced resistance: emerging experimental support for a slippery concept. Trends Plant Sci 7:61–67. https://doi.org/10.1016/S1360-1385(01)02186-0
Heiling S, Llorca LC, Li J, Gase K, Schmidt A, Schäfer M, Schneider B, Halitschke R, Gaquerel E, Baldwin IT (2021) Specific decorations of 17-hydroxygeranyllinalool diterpene glycosides solve the autotoxicity problem of chemical defense in Nicotiana attenuata. Plant Cell 33:1748–1770. https://doi.org/10.1093/plcell/koab048
Herms DA, Mattson WJ (1992) The dilemma of plants: To grow or defend. Q Rev Biol 67:282–335. http://www.jstor.org/stable/2830650
Hernández-García J, Briones-Moreno A, Blázquez MA (2021a) Origin and evolution of gibberellin signaling and metabolism in plants. Semin Cell Dev Biol 109:46–54. https://doi.org/10.1016/j.semcdb.2020.04.009
Hernández-García J, Sun R, Serrano-Mislata A, Inoue K, Vargas-Chávez C, Esteve-Bruna D, Arbona V, Yamaoka S, Nishihama R, Kohchi T et al (2021b) Coordination between growth and stress responses by DELLA in the liverwort Marchantia polymorpha. Curr Biol 31:1–9. https://doi.org/10.1016/j.cub.2021.06.010
Höll J, Lindner S, Walter H, Joshi D, Poschet G, Ziegler T, Hell R, Bogs J, Rausch T (2019) Impact of pulsed UV-B stress exposure on plant performance: How recovery periods stimulate secondary metabolism while reducing adaptive growth attenuation. Plant Cell Environ 42:801–8014. https://doi.org/10.1111/pce.13409
Hori K, Maruyama F, Fujisawa T, Togashi T, Yamamoto N, Seo M, Sato S, Yamada T, Mori H, Tajima N et al (2014) Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation. Nat Commun 5:3978. https://doi.org/10.1038/ncomms4978
Hou S, Thiergat T, Vannier N, Mesny F, Ziegler J, Pickel B, Hacquard S (2021) A microbiota-root-shoot circuit favours Arabidopsis growth over defence under suboptimal light. Nat Plants. https://doi.org/10.1038/s41477-021-00956-4
Huot B, Yao J, Montgomery BL, He SY (2014) Growth-defense tradeoffs in plants: a balancing act to optimize fitness. Mol Plant 7:1267–1287. https://doi.org/10.1093/mp/ssu049
Itkin M, Rogachev I, Alkan N, Rosenberg T, Malistky S, Masini L, Meir S, Iijima Y, Aoki K, de Vos R et al (2011) GLYCOALKALOID METABOLISM1 is required for steroidal alkaloid glycosylation and prevention of phytotoxicity in tomato. Plant Cell 23:4507–4525. https://doi.org/10.1105/tpc.111.088732
Jaremo J, Tuomi J, Nilsson P (1999) Adaptive status of localized and systemic defense responses in plants. In: Tollrian R, Harvell CD (eds) The ecology and evolution of inducible defenses. Princeton University Press, New Jersey
Jeschke V, Konrad W, Moore SS, Burow M (2019) Coordination of glucosinolate biosynthesis and turnover under different nutrient conditions. Front Plant Sci 10:1560. https://doi.org/10.3389/fpls.2019.01560
Johnson ET, Dowd PF (2004) Differentially enhanced insect resistance, at a cost, in Arabidopsis thaliana constitutively expressing a transcription factor of defensive metabolites. J Agr Food Chemi 52:5135–5138. https://doi.org/10.1021/jf0308049
Kang JH, Liu G, Shi F, Jones AD, Beaudry RM, Howe GA (2010) The tomato odorless-2 mutant is defective in trichome-based production of diverse specialized metabolites and broad-spectrum resistance to insect herbivores. Plant Physiol 154:262–272. https://doi.org/10.1104/pp.110.160192
Karasov TL, Chase E, Herman JJ, Bergelson J (2017) Mechanisms to mitigate the trade-off between growth and defense. Plant Cell 29:666–680. https://doi.org/10.1105/tpc.16.00931
Kazan K, Manners JM (2009) Linking development to defense: auxin in plant-pathogen interactions. Trends Plant Sci 14:373–382. https://doi.org/10.1016/j.tplants.2009.04.005
Kemen AC, Honkanen S, Melton RE, Findlay KC, Mugford ST, Hayashi K, Haralampidis K, Rosser SJ, Osbourn A (2014) Investigation of triterpene synthesis and regulation in oats reveals a role for b-amyrin in determining root epidermal cell patterning. Proc Natl Acad Sci USA 111:8679–8684. https://doi.org/10.1073/pnas.1401553111
Kessler A, Kalske A (2018) Plant secondary metabolite diversity and species interactions. Annu Rev Ecol Evol Syst 49:115–138. https://doi.org/10.1146/annurev-ecolsys-110617-062406
Kessler D, Diezel C, Baldwin IT (2010) Changing pollinators as means of escaping herbivores. Curr Biol 20:237–242. https://doi.org/10.1016/j.cub.2009.11.071
Kliebenstein DJ (2016) False idolatry of the mythical growth versus immunity tradeoff in molecular systems plant pathology. Physiol Mol Plant P 95:55–59. https://doi.org/10.1016/j.pmpp.2016.02.004
Kroymann J (2011) Natural diversity and adaptation in plant secondary metabolism. Curr Opin Plant Biol 14:246–251. https://doi.org/10.1016/j.pbi.2011.03.021
Kurashige NS, Agrawal AA (2005) Phenotypic plasticity to light competition and herbivory in Chenopodium album (Chenopodiaceae). Am J Bot 92:21–26. https://doi.org/10.3732/ajb.92.1.21
Kurokawa H, Kitahashi Y, Koike T, Lai J, Nakashizuka T (2002) Allocation to defense or growth in dipterocarp forest seedlings in Borneo. Oecologia 140:261–270. https://doi.org/10.1007/s00442-004-1566-7
Labandeira C (2007) The origin of herbivory on land: initial patterns of plant tissue consumption by arthropods. Insect Sci 14:259–275. https://doi.org/10.1111/j.1744-7917.2007.00141.x-i1
Laursen T, Moller BL, Bassard JE (2015) Plasticity of specialized metabolism as mediated by dynamic metabolons. Trends Plant Sci 20:20–32. https://doi.org/10.1016/j.tplants.2014.11.002
Leone M, Keller MM, Cerrudo I, Ballaré CL (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 204:355–367. https://doi.org/10.1111/nph.12971
Li J, Halitschke R, Li D, Paetz C, Su H, Heiling S, Xu S, Baldwin IT (2021) Controlled hydroxylations of diterpenoids allow for plant chemical defenses without autotoxicity. Science 371:255–260. https://doi.org/10.1126/science.abe4713
Lindroth RL, Batzli GO (1984) Plant phenolics as chemical defenses: effects of natural phenolics on survival and growth of prairie voles (Microtus ochrogaster). J Chem Ecol 10:229–244. https://doi.org/10.1007/BF00987851
Liu B, Seong K, Pang S, Song J, Gao H, Wang C, Zhan J, Zhang Y, Gao S, Li X et al (2021) Functional specificity, diversity, and redundancy of Arabidopsis JAZ family repressors in jasmonate and COI1-regulated growth, development, and defense. New Phytol. https://doi.org/10.1111/nph.17477
Liu Z, Carpenter SB, Bourgeois WJ, Yu Y, Constantin RJ, Falcon MJ, Adams JC (1998) Variations in the secondary metabolite camptothecin in relation to tissue age and season in Camptotheca acuminata. Tree Physiol 18:265–270. https://doi.org/10.1093/treephys/18.4.265
Major IT, Guo Q, Zhai J, Kapali G, Kramer DM, Howe GA (2020) A phytochrome B-independent pathway restricts growth at high levels of jasmonate defense. Plant Physiol 183:733–749. https://doi.org/10.1104/pp.19.01335
Major IT, Yoshida Y, Campos ML, Kapali G, Xin XF, Sugimoto K, Ferreira DO, He SY, Howe GA (2017) Regulation of growth-defense balance by JASMONATE ZIM-DOMAIN (JAZ)-MYC transcriptional module. New Phytol 215:1533–1547. https://doi.org/10.1111/nph.14638
Malitsky S, Bluem E, Less H, Venger I, Elbaz M, Morin S, Eshed Y, Aharoni A (2008) The transcript and metabolite networks affected by two clades of Arabidopsis glucosinolate biosynthesis regulators. Plant Physiol 148:2021–2049. https://doi.org/10.1104/pp.108.124784
Malone LA, Barraclough EI, Lin-Wang K, Stevenson DE, Allan AC (2009) Effects of red-leaved transgenic tobacco expressing a MYB transcription factor on two herbivorous insects, Spodoptera litura and Helicoverpa armigera. Entomol Exp Appl 133:117–127. https://doi.org/10.1111/j.1570-7458.2009.00910.x
Manhães AP, Veiga-Júnior VF, Wiedemann LSM, Fernandes KS, Sampaio PTB (2012) Biomass production and essential oil yield from leaves, fine stems and resprouts using pruning the crown of Aniba canelilla (H.B.K.) (Lauraceae) in the Central Amazon. Acta Amaz 42:355–362. https://doi.org/10.1590/S0044-59672012000300007
Martinez-Medina A, Flors V, Heil M, Mauch-Mani B, Pieterse CMJ, Pozo MJ, Ton J, van Dam NM, Conrath U (2016) Recognizing plant defense priming. Trends Plant Sci 21:818–822. https://doi.org/10.1016/j.tplants.2016.07.009
Mauch-Mani B, Baccelli I, Luna E, Flors V (2017) Defense priming: an adaptive part of induced resistance. Annu Rev Plant Biol 68:485–512. https://doi.org/10.1146/annurev-arplant-042916-041132
McGuire R, Agrawal AA (2005) Trade-offs between the shade-avoidance response and plant resistance to herbivores? Tests with mutant Cucumis sativus. Funct Ecol 19:1025–1031. https://doi.org/10.1111/j.1365-2435.2005.01047.x
Meier K, Ehbrecht MD, Wittstock U (2019) Glucosinolate content in dormant and germinating Arabidopsis thaliana seeds is affected by non-functional alleles of classical myrosinase and nitrile-specifier protein genes. Front Plant Sci 10:1549. https://doi.org/10.3389/fpls.2019.01549
Michael TP, Ernst E, Hartwick N, Chu P, Bryant D, Gilbert S, Ortleb S, Baggs EL, Sree KS, Appenroth KJ et al (2021) Genome and time-of-day transcriptome of Wolffia australiana link morphological minimization with gene loss and less growth control. Gen Res 31:225–238. https://doi.org/10.1101/gr.266429.120
Mihaliak CA, Lincoln DE (1989) Plant biomass partitioning and chemical defense: response to defoliation and nitrate limitation. Oecologia 80:122–126. https://doi.org/10.1007/BF00789940
Moreira X, Zas R, Solla A, Sampedro L (2015) Differentiation of persistent anatomical defensive structures is costly and determined by nutrient availability and genetic growth-defense tradeoffs. Tree Physiol 35:112–123. https://doi.org/10.1093/treephys/tpu106
Moreno JE, Tao Y, Chori J, Ballare CL (2009) Ecological modulation of plant defense via phytochrome control of jasmonate sensitivity. Proc Natl Acad Sci USA 106:4935–4940. https://doi.org/10.1073/pnas.0900701106
Morris JL, Puttick MN, Clark JW, Edwards D, Kenrick P, Pressel S, Wellman CH, Yang Z, Schneider H, Donoghue PCJ (2018) The timescale of early land plant evolution. Proc Natl Acad Sci USA 115:E2274–E2283. https://doi.org/10.1073/pnas.1719588115
Mukherjee S, Stamatis D, Bertsch J, Ovchinnikova G, Sundaramurthi JG, Lee J, Kandimalla M, Chen IMA, Kyrpides NC, Reddy TBK (2021) Genomes Online Database (GOLD) v.8: overview and updates. Nucleic Acids Res 49:D723–D733. https://doi.org/10.1093/nar/gkaa983
Mylona P, Owatworakit A, Papadopoulou K, Jenner H, Qin B, Findlay K, Hill L, Qi X, Bakht S, Melton R, Osbourn A (2008) Sad3 and Sad4 are required for saponin biosynthesis and root development in oat. Plant Cell 20:201–212. https://doi.org/10.1105/tpc.107.056531
Neilson EH, Goodger JQD, Woodrow IE, Moller BL (2013) Plant chemical defenses: at what cost? Trends Plant Sci 18:250–258. https://doi.org/10.1016/j.tplants.2013.01.001
Ohnmeiss TE, Baldwin IT (2000) Optimal defense theory predicts the ontogeny of an induced nicotine defense. Ecology 81:1765–1783. https://doi.org/10.1890/0012-9658
Prado A, Sierra A, Windsor D, Bede JC (2014) Leaf traits and herbivory levels in a tropical gymnosperm, Zamia stevensonii (Zamiaceae). Am J Bot 101:437–447. https://doi.org/10.3732/ajb.1300337
Purrington CB (2000) Costs of resistance. Curr Opin Plant Biol 3:305–308. https://doi.org/10.1016/S1369-5266(00)00085-6
Rasher DB, Hay ME (2014) Competition induces allelopathy but suppresses growth and anti-herbivore defence in chemically rich seaweed. Proc R Soc B 281:20132615. https://doi.org/10.1098/rspb.2013.2615
Rensing SA, Lang D, Zimer AD, Terry A, Salamov A, Shapiro H, Nishiyama T, Perroud PF, Lindquist EA, Kamisugi Y et al (2008) The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319:64–69. DOI: https://doi.org/10.1126/science.1150646
Sampedro L, Moreira X, Zas R (2011) Costs of constitutive and herbivore-induced chemical defenses in pine trees emerge only under low nutrient availability. J Ecol 99:818–827. https://doi.org/10.1111/j.1365-2745.2011.01814.x
Savary S, Willocquet L, Pethybridge SJ, Esker P, McRoberts N, Nelson A (2019) The global burden of pathogens and pests on major food crops. Nat Ecol Evol 3:430–439. https://doi.org/10.1038/s41559-018-0793-y
Schardl CL, Young CA, Pan J, Florea S, Takach JE, Panaccione DG, Farman ML, Webb JS, Jaromczyk J, Charlton ND et al (2013) Currencies of mutualisms: sources of alkaloid genes in vertically transmitted epichloae. Toxins 5:1064–1088. https://doi.org/10.3390/toxins5061064
Schilmiller AL, Stout J, Weng JK, Humphreys J, Ruegger MO, Chapple C (2009) Mutations in the cinnamate 4-hydroxylase gene impact metabolism, growth and development in Arabidopsis. Plant J 60:771–782. https://doi.org/10.1111/j.1365-313X.2009.03996.x
Schluttenhofer C (2020) Origin and evolution of jasmonate signaling. Plant Sci 298:110542. https://doi.org/10.1016/j.plantsci.2020.110542
Schultz JC, Baldwin IT (1982) Oak leaf quality declines in response to defoliation by gypsy moth larvae. Science 217:149–151. https://doi.org/10.1126/science.217.4555.149
Schwachtje J, Baldwin IT (2008) Why does herbivore attack reconfigure primary metabolism? Plant Phys 146:845–851. https://doi.org/10.1104/pp.107.112490
Shurin JB, Gruner DS, Hillebrand H (2006) All wet or dried up? Real differences between aquatic and terrestrial food webs. Proc R Soc B 273:1–9. https://doi.org/10.1098/rspb.2005.3377
Siemens DH, Garner SH, Mitchell-Olds T, Callaway RM (2002) Cost of defense in the context of plant competition: Brassica rapa may grow and defend. Ecology 83:505–517. https://doi.org/10.1890/0012-9658(2002)083[0505:CODITC]2.0.CO;2
Singh HP, Batish DR, Kohlu RK (1999) Autotoxicity: Concept, organisms, and ecological significance. Crit Rev Plant Sci 18:757–772. https://doi.org/10.1080/07352689991309478
Sirikantaramas S, Yamazaki M, Saito K (2008) Mutations in topoisomerase I as a self-resistance mechanism coevolved with the production of the anticancer alkaloid camptothecin in plants. Proc Natl Acad Sci USA 105:6782–6786. https://doi.org/10.1073/pnas.0801038105
Smet I, Voss U, Lau S, Wilson M, Shao N, Timme RE, Swarup R, Kerr I, Hogman C, Bock R et al (2011) Unraveling the evolution of auxin signaling. Plant Phys 155:209–211. https://doi.org/10.1104/pp.110.168161
Staker BL, Hjerrild K, Feese MD, Behnke CA, Burgin AB Jr, Stewart L (2002) The mechanism of topoisomerase I poisoning by camptothecin analog. Proc Natl Acad Sci USA 99:15387–15392. https://doi.org/10.1073/pnas.242259599
Tan S, Abas M, Verstraeten I, Glanc M, Molnár G, Hajny J, Lasák O, Petrik I, Russinova E, Petrásek J et al (2020) Salicylic acid targets protein phosphatase 2A to attenuate growth in plants. Curr Biol 30:381–395e8. https://doi.org/10.1016/j.cub.2019.11.058
Toth GB, Pavia H (2007) Induced herbivore resistance in seaweeds: a meta-analysis. J Ecol 95:425–434. https://doi.org/10.1111/j.1365-2745.2007.01224.x
Walters DR, Paterson L, Walsh DJ, Havis ND (2008) Priming for plant defense in barley provides benefits only under high disease pressure. Phys Mol Plant Pathol 73:95–100. https://doi.org/10.1016/j.pmpp.2009.03.002
Weng JK (2014) The evolutionary path towards complexity: a metabolic perspective. New Phytol 201:1141–1149. https://doi.org/10.1111/nph.12416
Wilkinson SW, Mageroy MH, Sánchez AL, Smith LM, Furci L, Cotton TEA, Krokene P, Ton J (2019) Surviving in a hostile world: plant strategies to resist pests and diseases. Annu Rev Phytopathol 57:505–529. https://doi.org/10.1146/annurev-phyto-082718-095959
Wink M (2008) Plant secondary metabolism: diversity, function and its evolution. Nat Prod Commun 3:1205–1216. https://doi.org/10.1177/1934578X0800300801
Yamamura C, Mizutani E, Okada K, Nakagawa H, Fukushima S, Tanaka A, Maeda S, Kamakura T, Yamane H, Takatsuji H (2015) Diterpenoid phytoalexin factor, a bHLH transcription factor, plays a central role in the biosynthesis of diterpenoid phytoalexins in rice. Plant J 84:1100–1113. https://doi.org/10.1111/tpj.13065
Yamasaki K, Kigawa T, Seki M, Shinozaki K, Yokoyama S (2013) DNA-binding transcription factors: structure, function, and evolution. Trends Plant Sci 18:267–276. https://doi.org/10.1016/j.tplants.2012.09.001
Yang DL, Yao J, Mei CS, Tong XH, Zeng LJ, Li Q, Xiao LT, Sun TP, Li J, Deng XW et al (2012) Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade. Proc Nat Acad Sci USA 109:E1192–E1200. https://doi.org/10.1073/pnas.1201616109
Yip EC, Tooker JF, Mescher MC, de Moraes CM (2019) Costs of plant defense priming: exposure to volatile cues from a specialist herbivore increases short-term growth but reduces rhizome production in tall goldenrod (Solidago altissima). BMC Plant Biol 19:209. https://doi.org/10.1186/s12870-019-1820-0
Younginger BS, Sirová D, Cruzan MB, Ballhorn DJ (2017) Is biomass a reliable estimate of plant fitness? Appl Plant Sci 5:1600094. https://doi.org/10.3732/apps.1600094
Zangerl AR, Arntz AM, Berenbaum MR (1997) Physiological price of an induced chemical defense: photosynthesis, respiration, biosynthesis, and growth. Oecologia 109:433–441. https://doi.org/10.1007/s004420050103
Zunjarrao SS, Tellis MB, Joshi SN, Joshi RS (2020) Plant-insect interaction: The saga of molecular coevolution. In: Mérillon JM, Ramawat K (eds) Co-evolution of secondary metabolites. Reference series in phytochemistry. Springer, Cham. https://doi.org/10.1007/978-3-319-96397-6_42
Züst T, Agrawal AA (2017) Trade-offs between plant growth and defense against insect herbivory: an emerging mechanistic synthetic. Annu Rev Plant Biol 68:513–534. https://doi.org/10.1146/annurev-arplant-042916-040856
Züst T, Rasmann S, Agrawal AA (2015) Growth-defense tradeoffs for two major anti-herbivore traits of the common milkweed Asclepias syriaca. Oikos 124:1404–1415. https://doi.org/10.1111/oik.02075
Züst T, Heichinger C, Grossniklaus U, Harrington R, Kliebenstein DJ, Turnbull LA (2012) Natural enemies drive geographic variation in plant defenses. Science 338:116–119. https://doi.org/10.1126/science.1226397
Acknowledgements
We thank two anonymous reviewers for their valuable comments, which were very helpful in improving the quality of this manuscript. We also thank J. Karpinski for suggestions in the text.
Funding
Work in the Campos lab is supported by the Fundação de Amparo à Pesquisa do Estado de Mato Grosso (FAPEMAT Grant No. 0209246/2021) and the Research Dean Fellowship from Universidade Federal de Mato Grosso.
Author information
Authors and Affiliations
Contributions
Both authors contributed equally to this work.
Corresponding author
Ethics declarations
Conflict of interest
Authors declare that they have no conflict of interest.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
This article belongs to the Topical Collection: Molecular Biology of Chemical Defenses.
Rights and permissions
About this article
Cite this article
Sestari, I., Campos, M.L. Into a dilemma of plants: the antagonism between chemical defenses and growth. Plant Mol Biol 109, 469–482 (2022). https://doi.org/10.1007/s11103-021-01213-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11103-021-01213-0