Phytochromes inhibit hypocotyl negative gravitropism by regulating the development of endodermal amyloplasts through phytochrome-interacting factors

Abstract

Phytochromes are red and far-red light photoreceptors that regulate various aspects of plant development. One of the lessunderstood roles of phytochromes is the inhibition of hypocotyl negative gravitropism, which refers to the loss of hypocotyl gravitropism and resulting random growth direction in red or farred light. This light response allows seedlings to curve toward blue light after emergence from the soil and enhances seedling establishment in the presence of mulch. Phytochromes inhibit hypocotyl negative gravitropism by inhibiting four phytochrome-interacting factors (PIF1, PIF3, PIF4, PIF5), as shown by hypocotyl agravitropism of dark-grown pif1 pif3 pif4 pif5 quadruple mutants. We show that phytochromes inhibit negative gravitropism by converting starchfilled gravity-sensing endodermal amyloplasts to other plastids with chloroplastic or etioplastic features in red or far-red light, whereas PIFs promote negative gravitropism by inhibiting the conversion of endodermal amyloplasts to etioplasts in the dark. By analyzing transgenic plants expressing PIF1 with an endodermisspecific SCARECROW promoter, we further show that endodermal PIF1 is sufficient to inhibit the conversion of endodermal amyloplasts to etioplasts and hypocotyl negative gravitropism of the pif quadruple mutant in the dark. Although the functions of phytochromes in gravitropism and chloroplast development are normally considered distinct, our results indicate that these two functions are closely related.

PIFs: Systems Integrators in Plant Development

“…Whereas dark-grown wild-type seedlings display normal skotomorphogenic development, etiolated pifq mutants resemble a wild-type seedling grown in the light, including short agravitropic hypocotyls and expanded cotyledons that contain developed chloroplast (Leivar et al, 2009;Shin et al, 2009;Kim et al, 2011). These data suggest that removal of these PIFs (by phy-induced degradation in the light in the wild type or genetically in the dark in pifq) underlies the seedling deetiolation response.…”

HUA ENHANCER1 Is Involved in Posttranscriptional Regulation of Positive and Negative Regulators in Arabidopsis Photomorphogenesis

“…Mutations in negative regulators of photomorphogenesis, such as CONSTITUTIVE PHOTOMORPHOGENIC1 (COP1) and PHYTOCHROME INTERACTING FACTORs (PIFs), also resulted in aberrant skotomorphogenic development, including short hypocotyl (Leivar and Quail, 2011), opened hook (Mazzella et al, 2014) and reduced antigravity responses (Kim et al, 2011). In the dark, hypocotyl lengths were shorter for the hen1-1 mutant than Ler ( Figure 1B).…”

The Photomorphogenic Signal: An Essential Component of Photoautotrophic Life

“…Phytochromes, through the action of PIFs, regulate the transition from amiloplasts to etioplasts and to chloroplasts. For example, the PIFs inhibit the conversion of endodermal amyloplasts to etioplasts, whereas the phytochromes antagonise this inhibition, promoting the formation of chloroplasts (Figure 3) (Kim et al, 2011).…”