Skip to main content
SpringerLink
Log in

Phylogenetic analysis of secondary metabolites in a plant community provides evidence for trade-offs between biotic and abiotic stress tolerance

  • Original Paper
  • Published:
Evolutionary Ecology Aims and scope Submit manuscript

Abstract

Plants' responses to conflicting stresses may result in physiological trade-offs due to the inter-dependent and costly nature of physiological investments. Physiological tradeoffs have been proved within species, but to what extent these trade-offs are the result of phylogenetic constraints remains poorly known. Environmental stresses can vary widely in different biomes, and therefore assessing physiological tradeoffs across species must account for this variation. One way of doing so is to assess it within a community, where the co-occurring species have faced a shared combination of filters to establish. Considering a representative sample of species in a single community, we use a macroevolutionary approach to test the hypothesis that plant physiological trade-offs are evolutionarily conserved within this community (i.e., closely-related species tend to solve the trade-offs similarly). We analyze the content of five metabolites in thirty co-occurring plant species, capturing their range of contrasting exposures to abiotic and biotic stresses (growing solitary and in vegetation patches). Our results support that species investment in response to abiotic stress (i.e., proline and abscisic acid content) is traded off against their investment to face biotic stress (i.e., jasmonic acid and salicylic acid), shown by the contrasting loadings of these two groups of metabolites in the first axes of a principal component analysis (PCA). In addition, the metabolic strategies observed in this community are evolutionarily conserved, as closely related species tend to have similar scores in this PCA, and thus resemble each other in their balance. This is shown by a significant phylogenetic signal in the species’ scores along the first axes of the PCA. Incorporating the evolutionary history of plant species into physiological studies can help to understand the response of plants to multiple stresses currently acting in ecological communities.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Ackerly DD (2003) Community assembly, niche conservatism, and adaptive evolution in changing environments. Int J Plant Sci 164:S165–S184

    Article  Google Scholar 

  • Anacker BL, Klironomos JN, Maherali H, Reinhart KO, Strauss SY (2014) Phylogenetic conservatism in plant-soil feedback and its implications for plant abundance. Ecol Lett 17:1613–1621

    Article  PubMed  Google Scholar 

  • Anderson JP, Badruzsaufari E, Schenk PM, Manners JM, Desmond OJ, Ehlert C et al (2004) Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. Plant Cell 16:3460–3479

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ariga H, Katori T, Tsuchimatsu T, Hirase T, Tajima Y, Parker JE et al (2017) NLR locus-mediated trade-off between abiotic and biotic stress adaptation in Arabidopsis. Nat Plants 3:17072

    Article  CAS  PubMed  Google Scholar 

  • Bates LS, Waldren RP, Teare I (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Berens ML, Wolinska KW, Spaepen S, Ziegler J, Nobori T, Nair A et al (2019) Balancing trade-offs between biotic and abiotic stress responses through leaf age-dependent variation in stress hormone cross-talk. Proc Natl Acad Sci 116:2364–2373

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blomberg SP, Garland JT, Ives AR, Crespi B (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57:717–745

    Article  PubMed  Google Scholar 

  • Bosch M, Wright LP, Gershenzon J, Wasternack C, Hause B, Schaller A, Stintzi A (2014) Jasmonic acid and its precursor 12-oxophytodienoic acid control different aspects of constitutive and induced herbivore defenses in tomato. Plant Physiol 166:396–410

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • CaraDonna PJ, Inouye DW (2015) Phenological responses to climate change do not exhibit phylogenetic signal in a subalpine plant community. Ecology 96:355–361

    Article  PubMed  Google Scholar 

  • Chang-Yang CH, Sun IF, Tsai CH, Lu CL, Hsieh CF (2016) ENSO and frost codetermine decade-long temporal variation in flower and seed production in a subtropical rain forest. J Ecol 104:44–54

    Article  Google Scholar 

  • Chen L, Zheng Y, Gao C, Mi XC, Ma KP, Wubet T, Guo LD (2017) Phylogenetic relatedness explains highly interconnected and nested symbiotic networks of woody plants and arbuscular mycorrhizal fungi in a Chinese subtropical forest. Mol Ecol 26:2563–2575

    Article  CAS  PubMed  Google Scholar 

  • Delalandre L, Montesinos-Navarro A (2018) Can co-occurrence networks predict plant-plant interactions in a semi-arid gypsum community? Perspect Plant Ecol Evol Syst 31:36–43

    Article  Google Scholar 

  • Durgbanshi A, Arbona V, Pozo O, Miersch O, Sancho JV, Gómez-Cadenas A (2005) Simultaneous determination of multiple phytohormones in plant extracts by liquid chromatographyelectrospray tandem mass spectrometry. J Agric Food Chem 53:8437–8442

    Article  CAS  PubMed  Google Scholar 

  • De Vos M, Van Zaanen W, Koornneef A, Korzelius JP, Dicke M, Van Loon L et al (2006) Herbivore-induced resistance against microbial pathogens in Arabidopsis. Plant Physiol 142:352–363

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • De Torres ZM, Bennett MH, Truman WH, Grant MR (2009) Antagonism between salicylic and abscisic acid reflects early host-pathogen conflict and moulds plant defence responses. Plant J 59:375–386

    Article  CAS  Google Scholar 

  • Dobra J, Motyka V, Dobrev P, Malbeck J, Prasil IT, Haisel D, Gaudinovaa A, Havlovaa M, Gubis J, Vankova R (2010) Comparison of hormonal responses to heat, drought and combined stress in tobacco plants with elevated proline content. J Plant Physiol 167:1360–1370

    Article  CAS  PubMed  Google Scholar 

  • Edwards EJ, Still CJ, Donoghue MJ (2007) The relevance of phylogeny to studies of global change. Trends Ecol Evol 22:243–249

    Article  PubMed  Google Scholar 

  • Epstein E, Ludwig-Müller J (1993) Indole-3-butyric acid in plants: occurrence, synthesis, metabolism and transport. Phys Plantarum 88:382–389

    Article  CAS  Google Scholar 

  • Eränen J, Nilsen J, Zverev V, Kozlov M (2009) Mountain birch under multiple stressors-heavy metal-resistant populations co-resistant to biotic stress but maladapted to abiotic stress. J Evol Biol 22:840–851

    Article  PubMed  Google Scholar 

  • Erb M, Meldau S, Howe GA (2012) Role of phytohormones in insect-specific plant reactions. Trends Plant Sci 17:250–259

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Foronda A, Pueyo Y, Arroyo AI, Saiz H, de la Luz GM, Alados CL (2019) The role of nurse shrubs on the spatial patterning of plant establishment in semi-arid gypsum plant communities. J Arid Environ 160:82–90

    Article  Google Scholar 

  • Fujita M, Fujit Y, Noutoshi Y, Takahashi F, Narusaka Y, Yamaguchi-Shinozaki K et al (2006) Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr Opin Plant Biol 9:436–442

    Article  PubMed  Google Scholar 

  • Gastauer M, Saporetti-Junior AW, Valladares F, Meira-Neto JA (2017) Phylogenetic community structure reveals differences in plant community assembly of an oligotrophic white-sand ecosystem from the Brazilian Atlantic Forest. Acta Bot Brasilica 31:531–538

    Article  Google Scholar 

  • Gilbert GS, Webb CO (2007) Phylogenetic signal in plant pathogen-host range. Proc Natl Acad Sci 104:4979–4983

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Ann Rev Phytopathol 43:205–227

    Article  CAS  Google Scholar 

  • Gómez JM, Verdú M, Perfectti F (2010) Ecological interactions are evolutionarily conserved across the entire tree of life. Nature 465:918–921

    Article  PubMed  CAS  Google Scholar 

  • Gómez-Cadenas A, Vives V, Zandalinas SI, Manzi M, Sanchez-Perez AM, Perez-Clemente RM, Arbona V (2015) Abscisic acid: a versatile phytohormone in plant signaling and beyond-current. Protein Peptide Sci 16:413–434

    Article  CAS  Google Scholar 

  • González-Orozco CE, Pollock LJ, Thornhill AH, Mishler BD, Knerr N, Laffan SW et al (2016) Phylogenetic approaches reveal biodiversity threats under climate change. Nat Clim Change 6:1110

    Article  Google Scholar 

  • Guan C, Cen HF, Cui X, Tian DY, Tadesse D, Zhang YW (2019) Proline improves switchgrass growth and development by reduced lignin biosynthesis. Sci Rep 9:1–8

    Google Scholar 

  • Hartmann M, Zeier J (2019) N-Hydroxypipecolic acid and salicylic acid: a metabolic duo for systemic acquired resistance. Curr Opin Plant Biol 50:44–57

    Article  CAS  PubMed  Google Scholar 

  • Hersh MH, Vilgalys R, Clark JS (2012) Evaluating the impacts of multiple generalist fungal pathogens on temperate tree seedling survival. Ecology 93:511–520

    Article  PubMed  Google Scholar 

  • Ives AR, Midford PE, Garland T (2007) Within-species variation and measurement error in phylogenetic comparative methods. Syst Biol 56:252–270

    Article  PubMed  Google Scholar 

  • Kissoudis C, Chowdhury R, van Heusden S, van de Wiel C, Finkers R, Visser RG et al (2015) Combined biotic and abiotic stress resistance in tomato. Euphytica 202:317–332

    Article  CAS  Google Scholar 

  • Klessig DF, Choi HW, Dempsey DMA (2018) Systemic acquired resistance and salicylic acid: past, present, and future. Mol Plant-microbe Interact 31:871–888

    Article  CAS  PubMed  Google Scholar 

  • Kluger CG, Dalling JW, Gallery RE, Sanchez E, Weeks-Galindo C, Arnold AE (2008) Host generalists dominate fungal communities associated with seeds of four neotropical pioneer species. J Trop Ecol 24:351–354

    Article  Google Scholar 

  • Kuntner M, Nuapuarucs M, Li D, Coddington JA (2014) Phylogeny predicts future habitat shifts due to climate change. PLoS ONE 9:e98907

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li X, Pei K, Kery M, Niklaus PA, Schmid B (2017) Decomposing functional trait associations in a Chinese subtropical forest. PLoS ONE 12(4):e0175727

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Makumburage GB, Richbourg HL, LaTorre KD, Capps A, Chen C, Stapleton AE (2013) Genotype to phenotype maps: multiple input abiotic signals combine to produce growth effects via attenuating signaling interactions in maize. G3 Genes Genom Genet 3:2195–2204

    Google Scholar 

  • Montesinos-Navarro A, Segarra-Moragues JG, Valiente-Banuet A, Verdú M (2012) Plant facilitation occurs between species differing in their associated arbuscular mycorrhizal fungi. New Phytol 196:835–844

    Article  CAS  PubMed  Google Scholar 

  • Munemasa S, Hauser F, Park J, Waadt R, Brandt B, Schroeder JI (2015) Mechanisms of abscisic acid-mediated control of stomatal aperture. Curr Opin Plant Biol 28:154–162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Münkemüller T, Boucher FC, Thuiller W, Lavergne S (2015) Phylogenetic niche conservatism–common pitfalls and ways forward. Funct Ecol 29:627–639

    Article  PubMed  PubMed Central  Google Scholar 

  • Novotny V, Basset Y (2005) Host specificity of insect herbivores in tropical forests. Proc R Soc B Biol Sci 272:1083–1090

    Article  Google Scholar 

  • Nagahama A, Yahara T (2019) Quantitative comparison of flowering phenology traits among trees, perennial herbs, and annuals in a temperate plant community. Am J Botany 106:1545–1557

    Article  Google Scholar 

  • Pearse IS, Aguilar J, Schroder J, Strauss SY (2017) Macroevolutionary constraints to tolerance: trade-offs with drought tolerance and phenology, but not resistance. Ecology 98:2758–2772

    Article  PubMed  Google Scholar 

  • Pihain M, Gerhold P, Ducousso A, Prinzing A (2019) Evolutionary response to coexistence with close relatives: increased resistance against specialist herbivores without cost for climatic-stress resistance. Ecol Lett 22:1285–1296

    PubMed  Google Scholar 

  • Qian H, Jin Y (2016) An updated megaphylogeny of plants, a tool for generating plant phylogenies and an analysis of phylogenetic community structure. J Plant Ecol 9:233–239

    Article  Google Scholar 

  • R Core Team (2018) R: A language and environment for statistical computing R Foundation for Statistical Computing. Vienna, Austria, https://www.R-project.org/

  • Rafferty NE, Nabity PD (2017) A global test for phylogenetic signal in shifts in flowering time under climate change. J Ecol 105:627–633

    Article  Google Scholar 

  • Revell LJ (2009) Size-correction and principal components for interspecific comparative studies. Evolution 63:3258–3268

    Article  PubMed  Google Scholar 

  • Revell LJ (2012) Phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 3:217–223

    Article  Google Scholar 

  • Ristok C, Poeschl Y, Dudenhӧffer JH, Ebeling A, Eisenhauer N, Vergara F et al (2019) Plant species richness elicits changes in the metabolome of grassland species via soil biotic legacy. J Ecol 107:2240–2254

    Article  Google Scholar 

  • Rivas-Ubach A, Barbeta A, Sardans J, Guenther A, Ogaya R, Oravec M et al (2016a) Topsoil depth substantially influences the responses to drought of the foliar metabolomes of Mediterranean forests. Perspect Plant Ecol Evol Syst 21:41–54

    Article  Google Scholar 

  • Rivas-Ubach A, Hódar JA, Sardans J, Kyle JE, Kim Y-M, Oravec M et al (2016b) Are the metabolomic responses to folivory of closely related plant species linked to macroevolutionary and plant-folivore coevolutionary processes? Ecol Evol 6:4372–4386

    Article  PubMed  PubMed Central  Google Scholar 

  • Rivas-Ubach A, Sardans J, Hódar JA, Garcia-Porta J, Guenther A, Pavsa-Tolic L et al (2017) Close and distant: contrasting the metabolism of two closely related subspecies of Scots pine under the effects of folivory and summer drought. Ecol Evol 7:8976–8988

    Article  PubMed  PubMed Central  Google Scholar 

  • Rivas-Ubach A, Sardans J, Pérez-Trujillo M, Estiarte M, Peñuelas J (2012) Strong relationship between elemental stoichiometry and metabolome in plants. Proc Natl Acad Sci 109:4181–4186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salazar A, Maschinski J, Possley J, Heineman K (2018) Seed germination of 53 species from the globally critically imperiled pine rockland ecosystem of South Florida, USA: effects of storage, phylogeny and life-history traits. Seed Sci Res 28:82–92

    Article  CAS  Google Scholar 

  • Sanchez DH, Schwabe F, Erban A, Udvardi MK, Kopka J (2012) Comparative metabolomics of drought acclimation in model and forage legumes. Plant Cell Environ 35:136–149

    Article  CAS  PubMed  Google Scholar 

  • Sah SK, Reddy KR, Li J (2016) Abscisic acid and abiotic stress tolerance in crop plants. Front Plant Sci 7:571

    Article  PubMed  PubMed Central  Google Scholar 

  • Sardans J, Penuelas J, Rivas-Ubach A (2011) Ecological metabolomics: overview of current developments and future challenges. Chemoecology 21:191–225

    Article  CAS  Google Scholar 

  • Simpson KJ, Ripley BS, Christin PA, Belcher CM, Lehmann CE, Thomas GH, Osborne CP (2016) Determinants of flammability in savanna grass species. J Ecol 104:138–148

    Article  PubMed  Google Scholar 

  • Spear ER, Mordecai EA (2018) Foliar pathogens are unlikely to stabilize coexistence of competing species in a California grassland. Ecology 99:2250–2259

    Article  PubMed  Google Scholar 

  • Thoen MP, Davila Olivas NH, Kloth KJ, Coolen S, Huang PP, Aarts MG, Bac-Molenaar JA, Bakker J, Bouwmeester HJ, Broekgaarden C et al (2017) Genetic architecture of plant stress resistance: multi-trait genome-wide association mapping. New Phytol 213:1346–1362

    Article  CAS  PubMed  Google Scholar 

  • Webb CO, Ackerly DD, McPeek MA, Donoghue MJ (2002) Phylogenies and community ecology. Ann Rev Ecol Syst 33:475–505

    Article  Google Scholar 

  • Werner GD, Cornwell WK, Sprent JI, Kattge J, Kiers ET (2014) A single evolutionary innovation drives the deep evolution of symbiotic N 2-fixation in angiosperms. Nat Commun 5:1–9

    Article  CAS  Google Scholar 

  • Ximénez-Embún MG, González-Guzmán M, Arbona V, Gómez-Cadenas A, Ortego F, Castañera P (2018) Plant-mediated effects of water deficit on the performance of Tetranychus evansi on tomato drought-adapted accessions. Front Plant Sci 9:1490

    Article  PubMed  PubMed Central  Google Scholar 

  • Zandalinas SI, Mittler R, Balfagón D, Arbona V, Gómez-Cadenas A (2018) Plant adaptations to the combination of drought and high temperatures. Physiol Plantarum 4:427–438

    Article  CAS  Google Scholar 

  • Zanne AE, Tank DC, Cornwell WK, Eastman JM, Smith SA, FitzJohn RG et al (2014) Three keys to the radiation of angiosperms into freezing environments. Nature 506:89–92

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

AMN was supported by a postdoctoral contract from the Spanish Ministry of Economy and Competitiveness (IJCI‐2015‐23498). RSM was supported by the Ministry of education and professional training, Spain (FPU Grant FPU17/00629). Financial support was provided by the Spanish Ministry of Economy and Competitiveness (RTI2018-099672-J-I00, AGL2016-76574-R). Hormone measurements were carried out at the central facilities (Servei Central d’Instrumentació Científica, SCIC) of the Universitat Jaume I. The Sapiencia Association and the Sanwei place facilitated and promoted the discussions that originated this work.

Author information

Authors and Affiliations

  1. Centro de Investigaciones Sobre Desertificación (CIDE, CSIC-UV-GV), Carretera de Moncada-Náquera, Km 4.5, 46113, Moncada, Valencia, Spain

    Alicia Montesinos-Navarro, Ricardo Sánchez-Martín & Miguel Verdú

  2. Departament de Ciències Agràries I del Medi Natural, Universitat Jaume I, Avda. Sos Baynat s/n, 12071, Castellón de la Plana, Spain

    Rosa M. Pérez-Clemente & Aurelio Gómez-Cadenas

Authors
  1. Alicia Montesinos-Navarro
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rosa M. Pérez-Clemente
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ricardo Sánchez-Martín
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Aurelio Gómez-Cadenas
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Miguel Verdú
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

AGC, MV and AMN planned and designed the research. AMN and RSM conducted fieldwork, RMPC and AGC performed the chemical analyses, AMN analyzed data. AMN wrote the first draft of the manuscript and all the authors contributed to the final version.

Corresponding author

Correspondence to Alicia Montesinos-Navarro.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 20 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Montesinos-Navarro, A., Pérez-Clemente, R.M., Sánchez-Martín, R. et al. Phylogenetic analysis of secondary metabolites in a plant community provides evidence for trade-offs between biotic and abiotic stress tolerance. Evol Ecol 34, 439–451 (2020). https://doi.org/10.1007/s10682-020-10044-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10682-020-10044-2

Keywords

Search

Navigation