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

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.