RuBPCase activase (RCA) mediates growth–defense trade‐offs: silencing RCA redirects jasmonic acid (JA) flux from JA‐isoleucine to methyl jasmonate (MeJA) to attenuate induced defense responses in Nicotiana attenuata

Summary RuBPCase activase (RCA), an abundant photosynthetic protein, is strongly down-regulated in response to Manduca sexta's oral secretion (OS) in Nicotiana attenuata. RCA-silenced plants are impaired not only in photosynthetic capacity and growth, but also in jasmonic acid-isoleucine (JA-Ile) signaling, and herbivore resistance mediated by JA-Ile-dependent defense traits. These responses are consistent with a resource-based growth–defense trade-off. As JA + Ile supplementation of OS restored wild-type (WT) levels of JA-Ile, defenses and resistance to M. sexta, but OS supplemented individually with JA or Ile did not, the JA-Ile deficiency of RCA-silenced plants could not be attributed to lower JA or Ile pools or JAR4/6 conjugating activity. Similar levels of JA-Ile derivatives after OS elicitation indicated unaltered JA-Ile turnover, and lower levels of other JA conjugates ruled out competition from other conjugation reactions. RCA-silenced plants accumulated more methyl jasmonate (MeJA) after OS elicitation, which corresponded to increased jasmonate methyltransferase (JMT) activity. RCA silencing phenocopies JMT overexpression, wherein elevated JMT activity redirects OS-elicited JA flux towards inactive MeJA, creating a JA sink which depletes JA-Ile and its associated defense responses. Hence, RCA plays an additional non-photosynthetic role in attenuating JA-mediated defenses and their associated costs, potentially allowing plants to anticipate resource-based constraints on growth before they actually occur.