As sessile organisms, plants constantly experience challenges from the surrounding environment. In response to these biotic stresses, plants invest a prominent portion of their metabolic capacity in the production of defense-associated compounds and physical structures. However, expression of defense traits is often associated with growth restriction and ultimately reduces reproductive output. Although this growth-defense antagonism has a profound impact on plant biology and agricultural practice, the mechanisms that regulate tradeoffs between growth and defense are poorly understood. The plant hormone jasmonate (JA) plays a dual role in enhancing immune responses and inhibiting growth. The JA signaling cascade is switched on when the bioactive form of the hormone is recognized by the COI1-JAZ co-receptor complex, which leads to the degradation of JAZ repressors via the SCFCOI1-26S proteasome pathway and subsequent relief of JA-responsive transcription factors (TFs). In this dissertation research, I first show that JAZ proteins promote growth and reproductive fitness in the model plant Arabidopsis thaliana by suppressing metabolic pathways for defense. Characterization of a jaz decuple (jazD) mutant defective in 10 JAZ genes revealed that hyperactivation of JA signaling significantly increased resource allocation to defense pathways, thereby improving plant resistance to insect herbivores and necrotrophic pathogens. The elevated defense of jazD was linked to carbon starvation, curtailed seed production and, under extreme conditions, lethality. Secondly, I show that the allocation costs associated with heightened JA responses in jazD was largely dependent on the bHLH-type TFs MYC2, MYC3 and MYC4, and that MYC2/3/4 played overlapping andconserved roles in metabolic reprogramming in jazD. Characterization of jazD myc mutants further showed that the JAZ-MYC transcriptional module controls the production of endoplasmic reticulum (ER)-derived structures called ER bodies, which are implicated in plant immunity. Finally, the jazD mutant was employed as a parental line in a genetic suppressor screen aimed at identification of novel mutations that uncouple growth-defense antagonism. Characterization of these suppressor of jazD (sjd) mutants revealed that JA signaling interacts with the red light signaling pathway to influence growth-defense balance. One sjd mutant (sjd56) not affected in red light signaling was also shown to partially uncouple growth-defense antagonism in jazD. Taken together, results from this dissertation provide evidence that growth-defense tradeoffs at low to moderate levels of defense are controlled by hardwired transcriptional networks, whereas high levels of defense inhibit growth through metabolic competition (allocation costs) between primary and secondary metabolism. Consistent with this view, JAZ proteins promote growth and reproductive fitness by preventing the negative effects of an unrestrained immune responses. The findings described in this dissertation may benefit the development of crop plants that are optimized for both growth and defense.
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