Plant Defense by Latex: Ecological Genetics of Inducibility in the Milkweeds and a General Review of Mechanisms, Evolution, and Implications for Agriculture

J Chem Ecol. 2019 Dec;45(11-12):1004-1018. doi: 10.1007/s10886-019-01119-8. Epub 2019 Nov 21.

Abstract

Latex occurs in 10% of plant families, has evolved independently many times, and is the most effective defense of milkweeds against its chewing herbivores. Here we report on new experiments on the heritability and inducibility of latex in several milkweed species. In addition, we review what is known about the genetic and environmental determinants of latex exudation, hormonal regulation, evolution within and among species, and the role and frequency of latex in agricultural crops. We first evaluated genotype-by-environment interactions using ~20 full-sibling genetic families in each of seven Asclepias species treated as controls or attacked by monarch butterfly caterpillars. All species showed substantial genetic variation for latex exudation and six of seven species responded to monarch herbivory (two species increased latex, two species decreased, and two showed variation among genetic families). Exogenous application of jasmonic acid (JA) to three species induced a consistent increase in latex (including species which showed a decline following caterpillar herbivory). We next evaluated three hypotheses for what determines genetic variation for induced latex in A. syriaca: 1) a trade-off with constitutive investment, 2) differential endogenous JA induction, or 3) variation in responsiveness to JA. We only found support for the second hypothesis: genetic families with a stronger JA-burst showed the greatest latex exudation following herbivory. We conclude that most species exhibit a genetic and inducible basis for latex, although genetic variation in inducibility is not pervasive. Finally, we summarized studies across 22 species of Asclepias and found that neither a species' latitude nor its phylogenetic position predicted latex inducibility. Nonetheless, a negative association between constitutive and induced latex across species indicates a macroevolutionary trade-off in allocation to this defense. Our review indicates that jasmonic acid is a key regulator of latex exudation, laticifer morphology, and defensive metabolites within latex. Biotic and abiotic factors strongly modulate latex expression. A survey of latex in food crops revealed that latex and analogous exudates (gums, resins, mucilage) are more common than expected based on their distribution across all plants. In conclusion, despite its widespread occurrence, the literature on latex is currently dominated by rubber trees and milkweeds, and we look forward to the broadening of ecological, agricultural, and mechanistic research into other systems.

Keywords: Asclepias; Jasmonic acid; Monarch butterfly Danaus plexippus; Phenotypic plasticity; Plant-insect interactions; Trade-offs.

MeSH terms

  • Animals
  • Asclepias / chemistry*
  • Butterflies / physiology
  • Crops, Agricultural
  • Cyclopentanes / chemistry
  • Cyclopentanes / metabolism
  • Genotype
  • Herbivory
  • Host-Parasite Interactions
  • Larva / metabolism
  • Latex / chemistry*
  • Latex / metabolism*
  • Male
  • Oxylipins / chemistry
  • Oxylipins / metabolism
  • Phylogeny
  • Plant Leaves / chemistry
  • Signal Transduction

Substances

  • Cyclopentanes
  • Latex
  • Oxylipins
  • jasmonic acid