CPR5-mediated nucleo-cytoplasmic localization of IAA12 and IAA19 controls lateral root development during abiotic stress.

Plasticity of the root system architecture (RSA) is essential in enabling plants to cope with various environmental stresses and is mainly controlled by the phytohormone auxin. Lateral root development is a major determinant of RSA. Abiotic stresses reduce auxin signaling output, inhibiting lateral root development; however, how abiotic stress translates into a lower auxin signaling output is not fully understood. Here, we show that the nucleo-cytoplasmic distribution of the negative regulators of auxin signaling AUXIN/INDOLE-3-ACETIC ACID INDUCIBLE 12 (AUX/IAA12 or IAA12) and IAA19 determines lateral root development under various abiotic stress conditions. The cytoplasmic localization of IAA12 and IAA19 in the root elongation zone enforces auxin signaling output, allowing lateral root development. Among components of the nuclear pore complex, we show that CONSTITUTIVE EXPRESSOR OF PATHOGENESIS-RELATED GENES 5 (CPR5) selectively mediates the cytoplasmic translocation of IAA12/19. Under abiotic stress conditions, CPR5 expression is strongly decreased, resulting in the accumulation of nucleus-localized IAA12/19 in the root elongation zone and the suppression of lateral root development, which is reiterated in the cpr5 mutant. This study reveals a regulatory mechanism for auxin signaling whereby the spatial distribution of AUX/IAA regulators is critical for lateral root development, especially in fluctuating environmental conditions.

JULGI-mediated increment in phloem transport capacity relates to fruit yield in tomato.

The continuous growth of the global population and the increase in the amount of arid land has severely constrained agricultural crop production. To solve this problem, many researchers have attempted to increase productivity through the efficient distribution of energy; however, the direct relationship between the plant vasculature, specifically phloem development, and crop yield is not well established. Here, we demonstrate that an optimum increase in phloem-transportation capacity by reducing SIJUL expression leads to improved sink strength in tomato (Solanum lycopersicum L.). SIJUL, a negative regulator of phloem development, suppresses the translation of a positive regulator of phloem development, SlSMXL5. The suppression of SlJUL increases the number of phloem cells and sucrose transport, but only an optimal reduction of SlJUL function greatly enhances sink strength in tomato, improving fruit setting, and yield contents by 37% and 60%, respectively. We show that the increment in phloem cell number confers spare transport capacity. Our results suggest that the control of phloem-transport capacity within the threshold could enhance the commitment of photosynthates to instigate yield improvement.

Translational control of phloem development by RNA G-quadruplex-JULGI determines plant sink strength.

The emergence of a plant vascular system was a prerequisite for the colonization of land; however, it is unclear how the photosynthate transporting system was established during plant evolution. Here, we identify a novel translational regulatory module for phloem development involving the zinc-finger protein JULGI (JUL) and its targets, the 5' untranslated regions (UTRs) of the SUPPRESSOR OF MAX2 1-LIKE4/5 (SMXL4/5) mRNAs, which is exclusively conserved in vascular plants. JUL directly binds and induces an RNA G-quadruplex in the 5' UTR of SMXL4/5, which are key promoters of phloem differentiation. We show that RNA G-quadruplex formation suppresses SMXL4/5 translation and restricts phloem differentiation. In turn, JUL deficiency promotes phloem formation and strikingly increases sink strength per seed. We propose that the translational regulation by the JUL/5' UTR G-quadruplex module is a major determinant of phloem establishment, thereby determining carbon allocation to sink tissues, and that this mechanism was a key invention during the emergence of vascular plants.