Downregulation of PHYTOCHROME-INTERACTING FACTOR 4 Influences Plant Development and Fruit Production

Abstract

Plant development is highly dependent on the ability to perceive and cope with environmental changes. In this context, PIF proteins are key players in the cellular hub controlling responses to fluctuating light and temperature conditions. Reports in various plant species show that manipulation of the PIF4 level affects important agronomical traits. In tomato (Solanum lycopersicum), SlPIF1a and SlPIF3 regulate fruit nutraceutical composition. However, the wider role of this protein family, and the potential of their manipulation for the improvement of other traits, has not been explored. Here we report the effects of constitutive silencing of tomato SlPIF4 on whole-plant physiology and development. Ripening anticipation and higher carotenoid levels observed in SlPIF4-silenced fruits revealed a redundant role of SlPIF4 in the accumulation of nutraceutical compounds. Furthermore, silencing triggered a significant reduction in plant size, flowering, fruit yield, and fruit size. This phenotype was most likely caused by reduced auxin levels and altered carbon partitioning. Impaired thermomorphogenesis and delayed leaf senescence were also observed in silenced plants, highlighting the functional conservation of PIF4 homologs in angiosperms. Overall, this work improves our understanding of the role of PIF proteins-and light signaling-in metabolic and developmental processes that affect yield and composition of fleshy fruits.

PIF4 Plays a Conserved Role in Solanum lycopersicum

“…Previous studies have demonstrated roles for SlPIF1a and SlPIF3 in tomato fruit ripening (Llorente et al, 2016;Gramegna et al, 2019). Rosado et al (2019) noticed that their SlPIF4 knockdown lines produced deepred fruit, which indicates that SlPIF4 likely suppresses tomato pigment production (Fig. 1).…”

“…In Arabidopsis, PIFs promote the transition to reproductive growth by directly upregulating the expression of the flowering inducer FT in the leaves (especially in the presence of shade or warm temperatures [Kumar et al, 2012;Galv ao et al, 2019]). Rosado et al (2019) demonstrate that their SlPIF4 knockdown lines have reduced FT in the leaves and an associated misregulation of floral transition genes in the shoot apex.…”

“…If we wish to convert our knowledge of Arabidopsis development into enhanced food security, it is essential that we investigate the conservation of these pathways in nutritionally relevant crops. In this issue of Plant Physiology, Rosado et al (2019) from the Magdalena Rossi lab at the University of São Paulo take a step toward doing so with a thorough characterization of PIF4 in tomato (Solanum lycopersicum).…”

“…AtPIF4 is particularly important in the control of plant architecture in response to warm temperatures (Koini et al, 2009). In the study published in this issue, Rosado et al (2019) set out to study the function of SlPIF4. They began by producing several RNA interference (RNAi) knockdown lines and confirmed that these lines show a reduced level of SlPIF4 expression.…”

“…More studies like that of Rosado et al (2019) will be needed in the coming years for us to understand how the plants we eat really grow. Their article highlights the extraordinary translatable value of research performed in Arabidopsis while also demonstrating its limitations.…”