Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Adaptive mechanisms of plant specialized metabolism connecting chemistry to function

Nature Chemical Biology volume 17, pages 1037–1045 (2021)Cite this article

Subjects

Abstract

As sessile organisms, plants evolved elaborate metabolic systems that produce a plethora of specialized metabolites as a means to survive challenging terrestrial environments. Decades of research have revealed the genetic and biochemical basis for a multitude of plant specialized metabolic pathways. Nevertheless, knowledge is still limited concerning the selective advantages provided by individual and collective specialized metabolites to the reproductive success of diverse host plants. Here we review the biological functions conferred by various classes of plant specialized metabolites in the context of the interaction of plants with their surrounding environment. To achieve optimal multifunctionality of diverse specialized metabolic processes, plants use various adaptive mechanisms at subcellular, cellular, tissue, organ and interspecies levels. Understanding these mechanisms and the evolutionary trajectories underlying their occurrence in nature will ultimately enable efficient bioengineering of desirable metabolic traits in chassis organisms.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: A brief history of phytochemistry research.
Fig. 2: Modes of below-ground biotic interaction mediated by plant specialized metabolism.
Fig. 3: Integration of plant specialized metabolism with body plan adaptation and growth regulation.
Fig. 4: Contribution of subcellular and intercellular mechanisms to the optimal multifunctionality of plant specialized metabolic processes.
Fig. 5: Evolutionary mechanisms contributing to novel plant specialized metabolic traits.

Similar content being viewed by others

References

  1. Kenrick, P. & Crane, P. R. The origin and early evolution of plants on land. Nature 389, 33–39 (1997).

    Article  CAS  Google Scholar 

  2. Li, F.-S. & Weng, J.-K. Demystifying traditional herbal medicine with modern approach. Nat. Plants 3, 17109 (2017).

    Article  PubMed  Google Scholar 

  3. De Smet, P. A. The role of plant-derived drugs and herbal medicines in healthcare. Drugs 54, 801–840 (1997).

    Article  PubMed  Google Scholar 

  4. Lau, W. & Sattely, E. S. Six enzymes from mayapple that complete the biosynthetic pathway to the etoposide aglycone. Science 349, 1224–1228 (2015). Leveraging coexpression analysis and transient transformation of N. benthamiana, the authors identify the biosynthetic pathway of the etoposide aglycone podophyllotoxin in mayapple.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Lichman, B. R. et al. The evolutionary origins of the cat attractant nepetalactone in catnip. Sci. Adv. 6, eaba0721 (2020). Using a comparative phylogenomics approach, the authors delineate the process underlying the reemergence of iridoid biosynthesis in catnip in the Nepeta lineage, which involves the assembly of a nepetalactone biosynthetic gene cluster.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Kessler, A. & Kalske, A. Plant secondary metabolite diversity and species interactions. Annu. Rev. Ecol. Evol. Syst. 49, 115–138 (2018).

    Article  Google Scholar 

  7. Bruce, T. J. A. & Pickett, J. A. Perception of plant volatile blends by herbivorous insects—finding the right mix. Phytochemistry 72, 1605–1611 (2011).

    Article  CAS  PubMed  Google Scholar 

  8. Kessler, D. et al. How scent and nectar influence floral antagonists and mutualists. eLife 4, e07641 (2015).

    Article  PubMed Central  Google Scholar 

  9. Erb, M. & Reymond, P. Molecular interactions between plants and insect herbivores. Annu. Rev. Plant Biol. 70, 527–557 (2019).

    Article  CAS  PubMed  Google Scholar 

  10. Mhlongo, M. I., Piater, L. A., Madala, N. E., Labuschagne, N. & Dubery, I. A. The chemistry of plant–microbe interactions in the rhizosphere and the potential for metabolomics to reveal signaling related to defense priming and induced systemic resistance. Front. Plant Sci. 9, 112 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  11. Schandry, N. & Becker, C. Allelopathic plants: models for studying plant-interkingdom interactions. Trends Plant Sci. 25, 176–185 (2020).

    Article  CAS  PubMed  Google Scholar 

  12. Weston, L. A. & Mathesius, U. Flavonoids: their structure, biosynthesis and role in the rhizosphere, including allelopathy. J. Chem. Ecol. 39, 283–297 (2013).

    Article  CAS  PubMed  Google Scholar 

  13. Voges, M. J. E. E. E., Bai, Y., Schulze-Lefert, P. & Sattely, E. S. Plant-derived coumarins shape the composition of an Arabidopsis synthetic root microbiome. Proc. Natl Acad. Sci. USA 116, 12558–12565 (2019).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Korenblum, E. et al. Rhizosphere microbiome mediates systemic root metabolite exudation by root-to-root signaling. Proc. Natl Acad. Sci. USA 117, 3874–3883 (2020). This work demonstrates that the tomato rhizosphere microbiome affects the chemical composition of root exudation through a systemic root–root signaling mechanism dubbed systemically induced root exudation of metabolites (SIREM).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Manohar, M. et al. Plant metabolism of nematode pheromones mediates plant–nematode interactions. Nat. Commun. 11, 208 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Hu, L. et al. Root exudate metabolites drive plant–soil feedbacks on growth and defense by shaping the rhizosphere microbiota. Nat. Commun. 9, 2738 (2018).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. Falik, O., Hoffmann, I. & Novoplansky, A. Say it with flowers: flowering acceleration by root communication. Plant Signal. Behav. 9, e28258 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  18. Huang, W., Zwimpfer, E., Hervé, M. R., Bont, Z. & Erb, M. Neighbourhood effects determine plant–herbivore interactions below-ground. J. Ecol. 106, 347–356 (2018).

    Article  CAS  Google Scholar 

  19. Rasmann, S. et al. Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434, 732–737 (2005).

    Article  CAS  PubMed  Google Scholar 

  20. Huang, W., Gfeller, V. & Erb, M. Root volatiles in plant–plant interactions. II. Root volatiles alter root chemistry and plant–herbivore interactions of neighbouring plants. Plant Cell Environ. 42, 1964–1973 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Gfeller, V. et al. Root volatiles in plant–plant interactions. I. High root sesquiterpene release is associated with increased germination and growth of plant neighbours. Plant Cell Environ. 42, 1950–1963 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Rand, K. et al. Differences in monoterpene biosynthesis and accumulation in Pistacia palaestina leaves and aphid-induced galls. J. Chem. Ecol. 43, 143–152 (2017).

    Article  CAS  PubMed  Google Scholar 

  23. Zhang, P.-J. et al. Airborne host–plant manipulation by whiteflies via an inducible blend of plant volatiles. Proc. Natl Acad. Sci. USA 116, 7387–7396 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Wang, X. et al. A novel Meloidogyne incognita chorismate mutase effector suppresses plant immunity by manipulating the salicylic acid pathway and functions mainly during the early stages of nematode parasitism. Plant Pathol. 67, 1436–1448 (2018).

    Article  CAS  Google Scholar 

  25. Lanver, D. et al. Ustilago maydis effectors and their impact on virulence. Nat. Rev. Microbiol. 15, 409–421 (2017).

    Article  CAS  PubMed  Google Scholar 

  26. Schuurink, R. & Tissier, A. Glandular trichomes: micro‐organs with model status? N. Phytol. 225, 2251–2266 (2020).

    Article  Google Scholar 

  27. Ramos, M. V., Demarco, D., da Costa Souza, I. C. & de Freitas, C. D. T. Laticifers, latex, and their role in plant defense. Trends Plant Sci. 24, 553–567 (2019).

    Article  CAS  PubMed  Google Scholar 

  28. Zhang, H., Wang, L., Deroles, S., Bennett, R. & Davies, K. New insight into the structures and formation of anthocyanic vacuolar inclusions in flower petals. BMC Plant Biol. 6, 29 (2006).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. Ngan, N. T. T. et al. Cytotoxic phenanthrenes and phenolic constituents from the tubers of Dioscorea persimilis. Phytochem. Lett. 40, 139–143 (2020).

    Article  CAS  Google Scholar 

  30. Levin, D. A. The role of trichomes in plant defense. Q. Rev. Biol. 48, 3–15 (1973).

    Article  Google Scholar 

  31. Livingston, S. J. et al. Cannabis glandular trichomes alter morphology and metabolite content during flower maturation. Plant J. 101, 37–56 (2020).

    Article  CAS  PubMed  Google Scholar 

  32. McDowell, E. T. et al. Comparative functional genomic analysis of Solanum glandular trichome types. Plant Physiol. 155, 524–539 (2011).

    Article  CAS  PubMed  Google Scholar 

  33. Leong, B. J. et al. Evolution of metabolic novelty: a trichome-expressed invertase creates specialized metabolic diversity in wild tomato. Sci. Adv. 5, eaaw3754 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Weinhold, A. & Baldwin, I. T. Trichome-derived O-acyl sugars are a first meal for caterpillars that tags them for predation. Proc. Natl Acad. Sci. USA 108, 7855–7859 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Hagel, J. M., Yeung, E. C. & Facchini, P. J. Got milk? The secret life of laticifers. Trends Plant Sci. 13, 631–639 (2008).

    Article  CAS  PubMed  Google Scholar 

  36. Bauer, G. et al. Investigating the rheological properties of native plant latex. J. R. Soc. Interface 11, 20130847 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  37. Singh, A., Menéndez-Perdomo, I. M. & Facchini, P. J. Benzylisoquinoline alkaloid biosynthesis in opium poppy: an update. Phytochem. Rev. 18, 1457–1482 (2019).

    Article  CAS  Google Scholar 

  38. Huber, M. et al. A latex metabolite benefits plant fitness under root herbivore attack. PLoS Biol. 14, e1002332 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  39. Abarca, L. F. S., Klinkhamer, P. G. L. & Choi, Y. H. Plant latex, from ecological interests to bioactive chemical resources. Planta Med. 85, 856–868 (2019).

    Article  CAS  Google Scholar 

  40. Freitas, C. D. T. et al. Identification, characterization, and antifungal activity of cysteine peptidases from Calotropis procera latex. Phytochemistry 169, 112163 (2020).

    Article  CAS  PubMed  Google Scholar 

  41. Konno, K. Plant latex and other exudates as plant defense systems: roles of various defense chemicals and proteins contained therein. Phytochemistry 72, 1510–1530 (2011).

    Article  CAS  PubMed  Google Scholar 

  42. Bernays, E. A., Singer, M. S. & Rodrigues, D. Trenching behavior by caterpillars of the Euphorbia specialist, Pygarctia roseicapitis: a field study. J. Insect Behav. 17, 41–52 (2004).

    Article  Google Scholar 

  43. Erb, M. & Kliebenstein, D. J. Plant secondary metabolites as defenses, regulators, and primary metabolites: the blurred functional trichotomy. Plant Physiol. 184, 39–52 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Lynch, J. H. et al. Modulation of auxin formation by the cytosolic phenylalanine biosynthetic pathway. Nat. Chem. Biol. 16, 850–856 (2020).

    Article  CAS  PubMed  Google Scholar 

  45. Kim, J. I., Zhang, X., Pascuzzi, P. E., Liu, C. & Chapple, C. Glucosinolate and phenylpropanoid biosynthesis are linked by proteasome-dependent degradation of PAL. N. Phytol. 225, 154–168 (2020). Analysis of the impact of indole glucosinolate intermediates on flux toward production of phenylpropanoids reveals the intertwined roles of metabolism, transcriptional control and protein turnover on co-regulation of distinct metabolic pathways.

    Article  CAS  Google Scholar 

  46. Katz, E. et al. The glucosinolate breakdown product indole-3-carbinol acts as an auxin antagonist in roots of Arabidopsis thaliana. Plant J. 82, 547–555 (2015).

    Article  CAS  PubMed  Google Scholar 

  47. Katz, E. & Chamovitz, D. A. Wounding of Arabidopsis leaves induces indole-3-carbinol-dependent autophagy in roots of Arabidopsis thaliana. Plant J. 91, 779–787 (2017).

    Article  CAS  PubMed  Google Scholar 

  48. Malinovsky, F. G. et al. An evolutionarily young defense metabolite influences the root growth of plants via the ancient TOR signaling pathway. eLife 6, e29353 (2017). Glucosinolates are specialized defense compounds produced by Brassicaceae plants against herbivores. This work identifies one of these glucosinolates, 3-hydroxypropylglucosinolate, that regulates root growth through influencing the TOR complex.

    Article  PubMed  PubMed Central  Google Scholar 

  49. Weng, J.-K., Ye, M., Li, B. & Noel, J. P. Co-evolution of hormone metabolism and signaling networks expands plant adaptive plasticity. Cell 166, 881–893 (2016).

    Article  CAS  PubMed  Google Scholar 

  50. Jia, K.-P. et al. Anchorene is a carotenoid-derived regulatory metabolite required for anchor root formation in Arabidopsis. Sci. Adv. 5, eaaw6787 (2019). A carotenoid-derived dialdehyde (diapocarotenoid) is identified as the specific signal needed for anchor root formation in Arabidopsis.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Ablazov, A. et al. The apocarotenoid zaxinone is a positive regulator of strigolactone and abscisic acid biosynthesis in Arabidopsis roots. Front. Plant Sci. 11, 578 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  52. Dickinson, A. J. et al. A plant lipocalin is required for retinal-mediated de novo root organogenesis. Preprint at bioRxiv https://doi.org/10.1101/2020.11.09.375444 (2020).

  53. Boachon, B. et al. Natural fumigation as a mechanism for volatile transport between flower organs. Nat. Chem. Biol. 15, 583–588 (2019). This work reveals the hormone-like function of terpenoids and their aerial transport within enclosed spaces of plant tissues, which impacts organ development and reproductive fitness.

    Article  CAS  PubMed  Google Scholar 

  54. Li, J. et al. The decoration of specialized metabolites influences stylar development. eLife 7, e38611 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  55. Alam, M. T. et al. The self-inhibitory nature of metabolic networks and its alleviation through compartmentalization. Nat. Commun. 8, 16018 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Knudsen, C., Gallage, N. J., Hansen, C. C., Møller, B. L. & Laursen, T. Dynamic metabolic solutions to the sessile life style of plants. Nat. Prod. Rep. 35, 1140–1155 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Schenck, C. A. & Last, R. L. Location, location! Cellular relocalization primes specialized metabolic diversification. FEBS J. 287, 1359–1368 (2020).

    Article  CAS  PubMed  Google Scholar 

  58. Widhalm, J. R. et al. Identification of a plastidial phenylalanine exporter that influences flux distribution through the phenylalanine biosynthetic network. Nat. Commun. 6, 8142 (2015).

    Article  PubMed  Google Scholar 

  59. Lynch, J. H. et al. Multifaceted plant responses to circumvent Phe hyperaccumulation by downregulation of flux through the shikimate pathway and by vacuolar Phe sequestration. Plant J. 92, 939–950 (2017).

    Article  CAS  PubMed  Google Scholar 

  60. Shitan, N. & Yazaki, K. Dynamism of vacuoles toward survival strategy in plants. Biochim. Biophys. Acta Biomembr. 1862, 183127 (2020).

    Article  CAS  PubMed  Google Scholar 

  61. Payne, R. M. E. et al. An NPF transporter exports a central monoterpene indole alkaloid intermediate from the vacuole. Nat. Plants 3, 16208 (2017).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  62. Rehm, F. B. H. et al. Papain-like cysteine proteases prepare plant cyclic peptide precursors for cyclization. Proc. Natl Acad. Sci. U. S. A. 116, 7831–7836 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Jackson, M. A. et al. Molecular basis for the production of cyclic peptides by plant asparaginyl endopeptidases. Nat. Commun. 9, 2411 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Brillouet, J.-M. et al. The tannosome is an organelle forming condensed tannins in the chlorophyllous organs of Tracheophyta. Ann. Bot. 112, 1003–1014 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Brillouet, J.-M. et al. Phenol homeostasis is ensured in vanilla fruit by storage under solid form in a new chloroplast-derived organelle, the phenyloplast. J. Exp. Bot. 65, 2427–2435 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Quilichini, T. D., Douglas, C. J. & Samuels, A. L. New views of tapetum ultrastructure and pollen exine development in Arabidopsis thaliana. Ann. Bot. 114, 1189–1201 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Kim, S. S. & Douglas, C. J. Sporopollenin monomer biosynthesis in Arabidopsis. J. Plant Biol. 56, 1–6 (2013).

    Article  CAS  Google Scholar 

  68. Onoyovwe, A. et al. Morphine biosynthesis in opium poppy involves two cell types: sieve elements and laticifers. Plant Cell 25, 4110–4122 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Li, W., Lybrand, D. B., Zhou, F., Last, R. L. & Pichersky, E. Pyrethrin biosynthesis: the cytochrome P450 oxidoreductase CYP82Q3 converts jasmolone to pyrethrolone. Plant Physiol. 181, 934–944 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Fu, X. et al. AaPDR3, a PDR transporter 3, is involved in sesquiterpene β-caryophyllene transport in Artemisia annua. Front. Plant Sci. 8, 723 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  71. Shibata, Y. et al. The full-size ABCG transporters Nb-ABCG1 and Nb-ABCG2 function in pre- and postinvasion defense against Phytophthora infestans in Nicotiana benthamiana. Plant Cell 28, 1163–1181 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Lefèvre, F. et al. The Nicotiana tabacum ABC transporter NtPDR3 secretes O-methylated coumarins in response to iron deficiency. J. Exp. Bot. 69, 4419–4431 (2018).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  73. Adebesin, F. et al. Emission of volatile organic compounds from petunia flowers is facilitated by an ABC transporter. Science 356, 1386–1388 (2017). This work shows that emission of volatile compounds out of cells relies on active transport and requires the action of an ATP-dependent transporter.

    Article  CAS  PubMed  Google Scholar 

  74. Liao, P. et al. Cuticle thickness affects dynamics of volatile emission from petunia flowers. Nat. Chem. Biol. 17, 138–145 (2021).

    Article  CAS  PubMed  Google Scholar 

  75. Barone, R. P. et al. The production of plant natural products beneficial to humanity by metabolic engineering. Curr. Plant Biol. 24, 100121 (2019).

    Article  Google Scholar 

  76. Achnine, L., Blancaflor, E. B., Rasmussen, S. & Dixon, R. A. Colocalization of l-phenylalanine ammonia-lyase and cinnamate 4-hydroxylase for metabolic channeling in phenylpropanoid biosynthesis. Plant Cell 16, 3098–3109 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Laursen, T. et al. Characterization of a dynamic metabolon producing the defense compound dhurrin in sorghum. Science 354, 890–893 (2016). By using styrene maleic acid copolymers, this work identifies the metabolon that produces the cyanogenic glucoside dhurrin in Sorghum bicolor.

    Article  CAS  PubMed  Google Scholar 

  78. Mucha, S. et al. The formation of a camalexin biosynthetic metabolon. Plant Cell 31, 2697–2710 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  79. Gou, M., Ran, X., Martin, D. W. & Liu, C.-J. The scaffold proteins of lignin biosynthetic cytochrome P450 enzymes. Nat. Plants 4, 299–310 (2018).

    Article  CAS  PubMed  Google Scholar 

  80. Zhang, Y. & Fernie, A. R. Metabolons, enzyme–enzyme assemblies that mediate substrate channeling, and their roles in plant metabolism. Plant Commun. 2, 100081 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  81. Chan, C. Y. et al. Microtubule-directed transport of purine metabolons drives their cytosolic transit to mitochondria. Proc. Natl Acad. Sci. USA 115, 13009–13014 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Branon, T. C. et al. Efficient proximity labeling in living cells and organisms with TurboID. Nat. Biotechnol. 36, 880–887 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Bar-Even, A. et al. The moderately efficient enzyme: evolutionary and physicochemical trends shaping enzyme parameters. Biochemistry 50, 4402–4410 (2011).

    Article  CAS  PubMed  Google Scholar 

  84. Copley, S. D. An evolutionary biochemist’s perspective on promiscuity. Trends Biochem. Sci. 40, 72–78 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Akashi, T., Aoki, T. & Ayabe, S.-I. Molecular and biochemical characterization of 2-hydroxyisoflavanone dehydratase. Involvement of carboxylesterase-like proteins in leguminous isoflavone biosynthesis. Plant Physiol. 137, 882–891 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Kruse, L. H. et al. Ancestral class-promiscuity as a driver of functional diversity in the BAHD acyltransferase family in plants. Preprint at bioRxiv https://doi.org/10.1101/2020.11.18.385815 (2020).

  87. Weng, J.-K. The evolutionary paths towards complexity: a metabolic perspective. N. Phytol. 201, 1141–1149 (2014).

    Article  Google Scholar 

  88. Zhang, J. Evolution by gene duplication: an update. Trends Ecol. Evol. 18, 292–298 (2003).

    Article  Google Scholar 

  89. Storme, N. D., De Storme, N. & Mason, A. Plant speciation through chromosome instability and ploidy change: cellular mechanisms, molecular factors and evolutionary relevance. Curr. Plant Biol. 1, 10–33 (2014).

    Article  Google Scholar 

  90. Shirai, K. & Hanada, K. Contribution of functional divergence through copy number variations to the inter-species and intra-species diversity in specialized metabolites. Front. Plant Sci. 10, 1567 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  91. Leong, B. J. & Last, R. L. Promiscuity, impersonation and accommodation: evolution of plant specialized metabolism. Curr. Opin. Struct. Biol. 47, 105–112 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Zhao, Q. et al. The reference genome sequence of Scutellaria baicalensis provides insights into the evolution of wogonin biosynthesis. Mol. Plant 12, 935–950 (2019).

    Article  CAS  PubMed  Google Scholar 

  93. Kaltenbach, M. et al. Evolution of chalcone isomerase from a noncatalytic ancestor. Nat. Chem. Biol. 14, 548–555 (2018).

    Article  CAS  PubMed  Google Scholar 

  94. Cridland, J. M., Majane, A. C., Sheehy, H. K. & Begun, D. J. Polymorphism and divergence of novel gene expression patterns in Drosophila melanogaster. Genetics 216, 79–93 (2020).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  95. Yona, A. H., Alm, E. J. & Gore, J. Random sequences rapidly evolve into de novo promoters. Nat. Commun. 9, 1530 (2018).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  96. Schläpfer, P. et al. Genome-wide prediction of metabolic enzymes, pathways, and gene clusters in plants. Plant Physiol. 173, 2041–2059 (2017).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  97. Banf, M., Zhao, K. & Rhee, S. Y. METACLUSTER—an R package for context-specific expression analysis of metabolic gene clusters. Bioinformatics 35, 3178–3180 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Nützmann, H.-W. et al. Active and repressed biosynthetic gene clusters have spatially distinct chromosome states. Proc. Natl Acad. Sci. USA 117, 13800–13809 (2020). This work reveals that plant biosynthetic gene clusters reside in highly interactive chromosomal domains that undergo marked changes in local conformation and nuclear positioning as a mechanism for co-regulation of genes in the cluster.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  99. Osbourn, A. Secondary metabolic gene clusters: evolutionary toolkits for chemical innovation. Trends Genet. 26, 449–457 (2010).

    Article  CAS  PubMed  Google Scholar 

  100. Yu, N. et al. Delineation of metabolic gene clusters in plant genomes by chromatin signatures. Nucleic Acids Res. 44, 2255–2265 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from the Keck Foundation (J.-K.W.), the Mathers Foundation (J.-K.W.), the Family Larsson-Rosenquist Foundation (J.-K.W.), the National Science Foundation (CHE-1709616 (J.-K.W.) and IOS-1655438 (N.D.)) and Agriculture Hatch (177845 (N.D.)). We thank V.W. Weng for assistance in scientific illustration.

Author information

Author notes

  1. Joseph H. Lynch

    Present address: Division of Plant and Soil Sciences, West Virginia University, Morgantown, WV, USA

Authors and Affiliations

  1. Whitehead Institute for Biomedical Research, Cambridge, MA, USA

    Jing-Ke Weng & Jason O. Matos

  2. Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, USA

    Jing-Ke Weng

  3. Department of Biochemistry, Purdue University, West Lafayette, IN, USA

    Joseph H. Lynch & Natalia Dudareva

  4. Purdue Center for Plant Biology, Purdue University, West Lafayette, IN, USA

    Joseph H. Lynch & Natalia Dudareva

Authors
  1. Jing-Ke Weng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Joseph H. Lynch
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jason O. Matos
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Natalia Dudareva
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Jing-Ke Weng or Natalia Dudareva.

Ethics declarations

Competing interests

J.-K.W. is a member of the scientific advisory board and a shareholder of DoubleRainbow Biosciences, Galixir and Inari Agriculture, which develop biotechnologies related to natural products, drug discovery and agriculture. All other authors have declared no competing interests.

Additional information

Peer review information Nature Chemical Biology thanks Matthias Erb and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Weng, JK., Lynch, J.H., Matos, J.O. et al. Adaptive mechanisms of plant specialized metabolism connecting chemistry to function. Nat Chem Biol 17, 1037–1045 (2021). https://doi.org/10.1038/s41589-021-00822-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41589-021-00822-6

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing