Lin Li

To over-top the neighbors, shade-intolerant plants trigger shade avoidance responses with increasing the elongation of stem-like organs at the expense of leaf development. Shade-induced elongation growth has been extensively studied, while the regulatory mechanisms underlying shade-suppressed leaf development remain poorly understood. Here we find sucrose can rescue shade-inhibited leaf development, which requires the functions of phytochrome A (phyA) and TARGET OF RAPAMYCIN (TOR) complex. We confirm an interaction between PHYA and LETHAL WITH SEC THIRTEEN 8 (LST8), a component of TOR complex. Shade and phyA affect TOR activity, in turn TOR affects the protein stability of PHYA. The sucrose-TOR mediated accumulation of PHYA requires CONSTITUTIVELY PHOTOMORPHOGENIC1 (COP1)/SUPPRESSOR OF PHYA-105 (SPA) complex. Transcriptome analysis further reveals that sucrose and phyA regulate the expression of leaf development-related genes under shade, particularly those involved in cytokinin metabolism. Our work uncovers a critical role for TOR and PHYA in linking light signaling with cellular energy status, a mechanism that fine-tunes leaf development specifically under shade conditions.

Amphibious plants escape submergence by plastically accelerating shoot growth, yet the mechanism underlying this convergent strategy remains unclear. Here, we demonstrate that PHYTOCHROME A (PHYA), a light photoreceptor, acts as a central regulator of the contrasting submergence escape capacities between amphibious Alternanthera philoxeroides and its terrestrial congener A. pungens. PHYA is distinctively regulated upon submergence in two congeners and negatively regulates submergence-induced elongation. Crucially, we find a cis-regulatory element (CRE) variant in the PHYA promoter between two congeners, which governs EIN3-dependent transcriptional repression and drives species-specific PHYA expression. Expanded investigation unveils phyletic retention of this CRE in other amphibious species, providing preliminary evidence for convergent evolution in the submergence escape capacity through independent co-option of the same CREs. Our findings demonstrate a role of PHYA in mediating submergence responses, deepen the understanding of the molecular basis for plant secondary aquatic adaptation, and inform flood-resilient crops engineering via cis-regulatory manipulation.

Shade avoidance syndrome (SAS) commonly occurs in plants sensing shading and the proximity of neighbors, leading to morphological and physiological changes that are detrimental to plant health and consequently crop yield. Controlling SAS could be beneficial for sustainable agriculture. Here, we performed a phenotype-based chemical screening in Arabidopsis and identified pifithrin-α (PFT-α) as a compound that suppresses shade-induced hypocotyl elongation and gene expression. Through genetic, biochemical, and molecular approaches, we demonstrated that PFT-α mimics ethylene by deactivating the ethylene receptor 1 (ETR1). Accumulated ethylene-insensitive 3 (EIN3) influences the expression of phytochrome-interacting factors ( PIF4 and PIF7 ) and subsequently inhibits shade-induced hypocotyl elongation. Our findings not only provide molecular insights into SAS but also suggest that PFT-α, acting as a potent ethylene mimic, plays a crucial role in hormone-regulated plant development and holds potential for modulating SAS in agricultural practices.

Shade avoidance helps plants maximize their access to light for growth under crowding. It is unknown, however, whether a priming shade avoidance mechanism exists that allows plants to respond more effectively to successive shade conditions. Here, we show that the shade-intolerant plant Arabidopsis can remember a first experienced shade event and respond more efficiently to the next event on hypocotyl elongation. The transcriptional regulator PHYTOCHROME-INTERACTING FACTOR 7 (PIF7) and the histone H3K27-demethylase RELATIVE OF EARLY FLOWERING 6 (REF6) are identified as being required for this shade avoidance memory. RNA-sequencing analysis reveals that shade induction of shade-memory-related genes is impaired in the pif7 and ref6 mutants. Based on the analyses of enrichments of H3K27me3, REF6 and PIF7, we find that priming shade treatment induces PIF7 accumulation, which further recruits REF6 to demethylate H3K27me3 on the chromatin of certain shade-memory-related genes, leading to a state poised for their transcription. Upon a second shade treatment, enhanced shade-mediated inductions of these genes result in stronger hypocotyl growth responses. We conclude that the transcriptional memory mediated by epigenetic modification plays a key role in the ability of primed plants to remember previously experienced shade and acquire enhanced responses to recurring shade conditions.

For shade-intolerant species, shade light indicates the close proximity of neighboring plants and triggers the shade avoidance syndrome (SAS), which causes exaggerated growth and reduced crop yield. Here, we report that non-secreted ROT FOUR LIKE (RTFL)/DEVIL (DVL) peptides negatively regulate SAS by interacting with BRASSINOSTEROID SIGNALING KINASEs (BSKs) and reducing the protein level of PHYTOCHROME INTERACTING FACTOR 4 (PIF4) in Arabidopsis. The transcription of at least five RTFLs (RTFL13/16/17/18/21) is induced by low R:FR light. The RTFL18 (DVL1) protein is stabilized under low R:FR conditions and localized to the plasma membrane. A phenotype analysis reveals that RTFL18 negatively regulates low R:FR-promoted petiole elongation. BSK3 and BSK6 are identified as partners of RTFL18 through binding assays and structural modeling. The overexpression of RTFL18 or knockdown of BSK3/6 reduces BRASSINOSTEROID signaling and reduces low R:FR-stabilized PIF4 levels. Genetically, the overexpression of BSK3/6 and PIF4 restores the petiole phenotype acquired by RTFL18-overexpressing lines. Collectively, our work characterizes a signaling cascade (the RTFLs-BSK3/6-PIF4 pathway) that prevents the excessive activation of the shade avoidance response in Arabidopsis.