Amyloplast sedimentation repolarizes LAZYs to achieve gravity sensing in plants.

Gravity controls directional growth of plants, and the classical starch-statolith hypothesis proposed more than a century ago postulates that amyloplast sedimentation in specialized cells initiates gravity sensing, but the molecular mechanism remains uncharacterized. The LAZY proteins are known as key regulators of gravitropism, and lazy mutants show striking gravitropic defects. Here, we report that gravistimulation by reorientation triggers mitogen-activated protein kinase (MAPK) signaling-mediated phosphorylation of Arabidopsis LAZY proteins basally polarized in root columella cells. Phosphorylation of LAZY increases its interaction with several translocons at the outer envelope membrane of chloroplasts (TOC) proteins on the surface of amyloplasts, facilitating enrichment of LAZY proteins on amyloplasts. Amyloplast sedimentation subsequently guides LAZY to relocate to the new lower side of the plasma membrane in columella cells, where LAZY induces asymmetrical auxin distribution and root differential growth. Together, this study provides a molecular interpretation for the starch-statolith hypothesis: the organelle-movement-triggered molecular polarity formation.

A minus-end directed kinesin motor directs gravitropism in Physcomitrella patens.

Gravity is a critical environmental factor regulating directional growth and morphogenesis in plants, and gravitropism is the process by which plants perceive and respond to the gravity vector. The cytoskeleton is proposed to play important roles in gravitropism, but the underlying mechanisms are obscure. Here we use genetic screening in Physcomitrella patens, to identify a locus GTRC, that when mutated, reverses the direction of protonemal gravitropism. GTRC encodes a processive minus-end-directed KCHb kinesin, and its N-terminal, C-terminal and motor domains are all essential for transducing the gravity signal. Chimeric analysis between GTRC/KCHb and KCHa reveal a unique role for the N-terminus of GTRC in gravitropism. Further study shows that gravity-triggered normal asymmetric distribution of actin filaments in the tip of protonema is dependent on GTRC. Thus, our work identifies a microtubule-based cellular motor that determines the direction of plant gravitropism via mediating the asymmetric distribution of actin filaments.

The Asymmetric Expression of SAUR Genes Mediated by ARF7/19 Promotes the Gravitropism and Phototropism of Plant Hypocotyls.

The asymmetric distribution of auxin leads to the bending growth of hypocotyls during gravitropic and phototropic responses, but the signaling events downstream of auxin remain unclear. Here, we identify many SAUR genes showing asymmetric expression in soybean hypocotyls during gravistimulation and then study their homologs in Arabidopsis. SAUR19 subfamily genes have asymmetric expression in Arabidopsis hypocotyls during gravitropic and phototropic responses, induced by the lateral redistribution of auxin. Both the mutation of SAUR19 subfamily genes and the ectopic expression of SAUR19 weaken these tropic responses, indicating the critical role of their asymmetric expression. The auxin-responsive transcription factor ARF7 may directly bind the SAUR19 promoter and activate SAUR19 expression asymmetrically in tropic responses. Taken together, our results reveal that a gravity- or light-triggered asymmetric auxin distribution induces the asymmetric expression of SAUR19 subfamily genes by ARF7 and ARF19 in the hypocotyls, which leads to bending growth during gravitropic and phototropic responses.

Arabidopsis PP6 phosphatases dephosphorylate PIF proteins to repress photomorphogenesis.

The PHYTOCHROME-INTERACTING FACTORs (PIFs) play a central role in repressing photomorphogenesis, and phosphorylation mediates the stability of PIF proteins. Although the kinases responsible for PIF phosphorylation have been extensively studied, the phosphatases that dephosphorylate PIFs remain largely unknown. Here, we report that seedlings with mutations in FyPP1 and FyPP3, 2 genes encoding the catalytic subunits of protein phosphatase 6 (PP6), exhibited short hypocotyls and opened cotyledons in the dark, which resembled the photomorphogenic development of dark-grown pifq mutants. The hypocotyls of dark-grown sextuple mutant fypp1 fypp3 (f1 f3) pifq were shorter than those of parental mutants f1 f3 and pifq, indicating that PP6 phosphatases and PIFs function synergistically to repress photomorphogenesis in the dark. We showed that FyPPs directly interacted with PIF3 and PIF4, and PIF3 and PIF4 proteins exhibited mobility shifts in f1 f3 mutants, consistent with their hyperphosphorylation. Moreover, PIF4 was more rapidly degraded in f1 f3 mutants than in wild type after light exposure. Whole-genome transcriptomic analyses indicated that PP6 and PIFs coregulated many genes, and PP6 proteins may positively regulate PIF transcriptional activity. These data suggest that PP6 phosphatases may repress photomorphogenesis by controlling the stability and transcriptional activity of PIF proteins via regulating PIF phosphorylation.

The Transcription Factors TCP4 and PIF3 Antagonistically Regulate Organ-Specific Light Induction of SAUR Genes to Modulate Cotyledon Opening during De-Etiolation in Arabidopsis.

Light elicits different growth responses in different organs of plants. These organ-specific responses are prominently displayed during de-etiolation. While major light-responsive components and early signaling pathways in this process have been identified, this information has yet to explain how organ-specific light responses are achieved. Here, we report that members of the TEOSINTE BRANCHED1, CYCLOIDEA, and PCF (TCP) transcription factor family participate in photomorphogenesis and facilitate light-induced cotyledon opening in Arabidopsis (Arabidopsis thaliana). Chromatin immunoprecipitation sequencing and RNA sequencing analyses indicated that TCP4 targets a number of SMALL AUXIN UPREGULATED RNA (SAUR) genes that have previously been shown to exhibit organ-specific, light-responsive expression. We demonstrate that TCP4-like transcription factors, which are predominantly expressed in the cotyledons of both light- and dark-grown seedlings, activate SAUR16 and SAUR50 expression in response to light. Light regulates the binding of TCP4 to the promoters of SAUR14, SAUR16, and SAUR50 through PHYTOCHROME-INTERACTING FACTORs (PIFs). PIF3, which accumulates in etiolated seedlings and its levels rapidly decline upon light exposure, also binds to the SAUR16 and SAUR50 promoters, while suppressing the binding of TCP4 to these promoters in the dark. Our study reveals that the interplay between light-responsive factors PIFs and the developmental regulator TCP4 determines the cotyledon-specific light regulation of SAUR16 and SAUR50, which contributes to cotyledon closure and opening before and after de-etiolation.

Ag nanoparticles inhibit the growth of the bryophyte, Physcomitrella patens.

The wide use of Ag nanoparticles (Ag NPs) as antimicrobial agents has resulted in a massive release of Ag NPs into environment, such as water and soil. As bryophytes live ubiquitously in water and soil, their tolerance and response to Ag NPs could be employed as an indicator for the harm of Ag NPs to the environment. Herein, we report the study on the physiological and biochemical responses of bryophytes to Ag NPs with different surface coatings at the gametophyte stages: protonema and leafy gametophyte, by using Physcomitrella patens as a model system. We found that Ag NPs, including AgNPs-B (Ag NPs without surface coating), AgNPs-PVP (Ag NPs coated with poly (N-vinyl-2-pyrrolidone)) and AgNPs-Cit (Ag NPs coated with citrate), were toxic to P. patens in terms of growth and development of the gametophyte. The toxicity was closely related to the concentration and surface coating of Ag NPs, and the growth stage of P. patens. The protonema was more sensitive to Ag NPs than the leafy gametophyte. Ag NPs inhibited the growth of the protonema following the trend of AgNPs-B > AgNPs-Cit > AgNPs-PVP. Ag NPs changed the thylakoid and chlorophyll contents, but did not affect the contents of essential elements in the protonema. At the leafy gametophyte stage, Ag NPs inhibited the growth of P. patens following a different order: AgNPs-Cit > AgNPs-B ≈ AgNPs-PVP. Ag NPs decreased the chlorophyll b content and disturbed the balance of some important essential elements in the leafy gametophytes. Both the dissolved fraction of Ag NPs and Ag NPs per se contributed to the toxicity. This study for the first time reveals the effects of Ag NPs on bryophytes at different growth stages, which calls for more attention to the nanoecotoxicology of Ag NPs.