Two‐tier morpho‐chemical defence tactic in Aethionema via fruit morph plasticity and glucosinolates allocation in diaspores

• Published in: Plant, cell and environment cell and environment, 2019-04, Vol.42 (4), p.1381-1392
• Main Authors: Bhattacharya, Samik, Mayland‐Quellhorst, Sara, Müller, Caroline, Mummenhoff, Klaus
• Format: Article
• Language: English
• Subjects: Bioassays; Brassicaceae; Brassicaceae - growth & development; Brassicaceae - metabolism; Chemical defense; dehiscent and indehiscent fruit morphs; Dimorphism; Dispersion; Fruit - growth & development; Fruit - metabolism; Fruits; Fungi; Glucosinolates; Glucosinolates - metabolism; Herbivory; herbivory, multivariate PCA; Indoles; Life history; Ontogeny; Optimization; Organic chemistry; Pericarp; plant defence compounds; Plutella xylostella; Progeny; Seed Dispersal; Seeds; Seeds - growth & development; Seeds - metabolism
• ISSN: 0140-7791; 1365-3040
• DOI: 10.1111/pce.13462

Fruit dimorphism and the production of glucosinolates (GSLs) are two specific life history traits found in the members of Brassicales, which aid to optimize seed dispersal and defence against antagonists, respectively. We hypothesized that the bipartite dispersal strategy demands a tight control over the production of fruit morphs with expectedly differential allocation of defensive anticipins (GSLs). In dimorphic Aethionema, herbivory by Plutella xylostella at a young stage triggered the production of more dehiscent (seeds released from fruit) than indehiscent fruit morphs (seeds enclosed within persistent pericarp) on the same plant upon maturity. Total GSL concentrations were highest in the mature seeds of dehiscent fruits from Aethionema arabicum and Aethionema saxatile among the different ontogenetic stages of the diaspores. Multivariate analyses of GSL profiles indicated significantly higher concentrations of specific indole GSLs in the diaspores, which require optimal defence after dispersal (i.e., seeds of dehiscent and fruit/pericarp of indehiscent fruit). Bioassays with a potentially coinhabitant fungus, Aspergillus quadrilineatus, support the distinct defensive potential of the diaspores corresponding to their GSL allocation. These findings indicate a two‐tier morpho‐chemical defence tactic of Aethionema via better protected fruit morphs and strategic provision of GSLs that optimize protection to the progeny for survival in nature. Plants, rooted and sessile, generally modify morphology (heteromorphy) and produce special metabolites (anticipins) as tactics to defend themselves and its progeny from the natural antagonists. We integrated the herbivore bioassay on mother plant to track plasticity of fruit morphs in dimorphic Aethionema (Brassicaceae) species and the state‐of‐the‐art metabolomics analyses to determine glucosinolates allocation at ontogenetic stages in the diaspores. Although herbivory triggered the production of more dehiscent than indehiscent fruits, indole glucosinolates were strategically allocated to the diaspores that demand maximum protection after dispersal. Our holistic approach led to the discovery of a two‐tier morpho‐chemical defence strategy in Aethionema for optimal fitness that complement the bet hedging strategy with dimorphic fruit.