N(6)-Methyladenosine (m(6)A) represents the most prevalent internal modification on mRNA and requires a multicomponent m(6)A methyltransferase complex in mammals. How their plant counterparts determine the global m(6)A modification landscape and its molecular link to plant development remain unknown. Here we show that FKBP12 INTERACTING PROTEIN 37 KD (FIP37) is a core component of the m(6)A methyltransferase complex, which underlies control of shoot stem cell fate in Arabidopsis. The mutants lacking FIP37 exhibit massive overproliferation of shoot meristems and a transcriptome-wide loss of m(6)A RNA modifications. We further demonstrate that FIP37 mediates m(6)A RNA modification on key shoot meristem genes inversely correlated with their mRNA stability, thus confining their transcript levels to prevent shoot meristem overproliferation. Our results suggest an indispensable role of FIP37 in mediating m(6)A mRNA modification, which is required for maintaining the shoot meristem as a renewable source for continuously producing all aerial organs in plants.
The spatiotemporal architecture of inflorescences that bear flowers determines plant reproductive success by affecting fruit set and plant interaction with pollinators. The inflorescence architecture that displays great diversity across flowering plants depends on developmental decisions at inflorescence meristems. Here we report a key conserved genetic pathway determining inflorescence architecture in Arabidopsis thaliana and Oryza sativa (rice). In Arabidopsis, four MADS-box genes, SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1, SHORT VEGETATIVE PHASE, AGAMOUS-LIKE 24, and SEPALLATA 4 act redundantly and directly to suppress TERMINAL FLOWER1 (TFL1) in emerging floral meristems. This is indispensable for the well-known function of APETALA1 in specifying floral meristems and is coupled with a conformational change in chromosome looping at the TFL1 locus. Similarly, we demonstrate that the orthologs of these MADS-box genes in rice determine panicle branching by regulating TFL1-like genes. Our findings reveal a conserved regulatory pathway that determines inflorescence architecture in flowering plants.
Flowering time is a critical agronomic trait that determines successful seed production and adaptation of crop plants. Photoperiodic control of this process in flowering plants is mediated by the long-distance mobile signal called florigen partly encoded by FLOWERING LOCUS T (FT) in Arabidopsis thaliana and its orthologs in other plant species. Despite the progress in understanding FT transport in the dicot model Arabidopsis, the mechanisms of florigen transport in monocots, which provide most of the biomass in agriculture, are unknown. Here, we show that rice FT-INTERACTING PROTEIN1 (OsFTIP1), a member of the family of multiple C2 domain and transmembrane region proteins (MCTPs) and the closest ortholog of Arabidopsis FTIP1, is required for export of RICE FLOWERING LOCUS T 1 (RFT1) from companion cells to sieve elements. This affects RFT1 movement to the shoot apical meristem and its regulation of rice flowering time under long days. We further reveal that a ubiquitin-like domain kinase g4, OsUbDKg4, interacts with OsFTIP1 and modulates its degradation in leaves through the 26S proteasome, which in turn affects RFT1 transport to the shoot apical meristem. Thus, dynamic modulation of OsFTIP1 abundance in leaves by a negative regulator OsUbDKg4 is integral to the role of OsFTIP1 in mediating RFT1 transport in rice and provides key evidence for a conserved role of FTIP1-like MCTPs in mediating florigen transport in flowering plants.
Organogenesis in higher plants occurs in the shoot meristem, which contains pluripotent stem cells. Here, we show that two multiple C2 domain and transmembrane region proteins, FT INTERACTING PROTEIN 3 (FTIP3) and FTIP4, play an essential role in mediating proliferation and differentiation of shoot stem cells in Arabidopsis. FTIP3/4 prevent intracellular trafficking of a key regulator, SHOOTMERISTEMLESS (STM), to the plasma membrane in cells in the peripheral shoot meristem region. This facilitates STM recycling to the nucleus to maintain stem cells. Without FTIP3/4, STM localizes substantially to the plasma membrane, which promotes intercellular trafficking but compromises nuclear localization of STM. This accelerates stem cell differentiation, causing early termination of shoot apices and resulting in dwarf and bushy phenotypes. Our findings reveal a molecular framework that determines the fate of shoot stem cells and the resulting aboveground plant body.
Multiple flowering pathways in Arabidopsis (Arabidopsis thaliana) converge on the transcriptional regulation of FLOWERING LOCUS T (FT), encoding a mobile floral stimulus that moves from leaves to the shoot apex. Despite our progress in understanding FT movement, the mechanisms underlying its transport along the endoplasmic reticulum-plasmalemma pathway in phloem companion cells remain largely unclear. Here, we show that the plasma membrane-resident syntaxin-like glutamine-soluble N-ethylmaleimide-sensitive factor protein attachment protein receptor (Q-SNARE), SYNTAXIN OF PLANTS121 (SYP121), interacts with QUIRKY (QKY), a member of the family of multiple C2 domain and transmembrane region proteins (MCTPs), to mediate FT transport in Arabidopsis. QKY and SYP121 coordinately regulate FT movement to the plasmalemma through the endosomal trafficking pathway and are required for FT export from companion cells to sieve elements, thus affecting FT transport through the phloem to the shoot apical meristem. These findings suggest that MCTP-SNARE complex-mediated endosomal trafficking is essential for the export of florigen from phloem companion cells to sieve elements to induce flowering.
Nuclear pore complexes (NPCs), which comprise multiple copies of nucleoporins (Nups), are large protein assemblies embedded in the nuclear envelope connecting the nucleus and cytoplasm. Although it has been known that Nups affect flowering in
Arabidopsis
, the underlying mechanisms are poorly understood. Here, we show that loss of function of
Nucleoporin 160
(
Nup160
) leads to increased abundance of CONSTANS (CO) protein and the resulting upregulation of
FLOWERING LOCUS T
(
FT
) specifically in the morning. We demonstrate that Nup160 regulates CO protein stability through affecting NPC localization of an E3-ubiquitin ligase, HIGH EXPRESSION OF OSMOTICALLY RESPONSIVE GENES1 (HOS1), which destabilizes CO protein in the morning period. Taken together, these results provide a mechanistic understanding of Nup function in the transition from vegetative to reproductive growth, suggesting that deposition of HOS1 at NPCs by Nup160 is essential for preventing precocious flowering in response to photoperiod in
Arabidopsis
.
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