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Plants have evolved a remarkable faculty of adaptation to deal with various and changing environmental conditions. In this context, the roots have taken over nutritional aspects and the root system architecture can be modulated in response to nutrient availability or biotic interactions with soil microorganisms. This adaptability requires a fine tuning of gene expression. Indeed, root specification and development are highly complex processes requiring gene regulatory networks involved in hormonal regulations and cell identity. Among the different molecular partners governing root development, microRNAs (miRNAs) are key players for the fast regulation of gene expression. miRNAs are small RNAs involved in most developmental processes and are required for the normal growth of organisms, by the negative regulation of key genes, such as transcription factors and hormone receptors. Here, we review the known roles of miRNAs in root specification and development, from the embryonic roots to the establishment of root symbioses, highlighting the major roles of miRNAs in these processes.

Key message This review summarizes recent knowledge on functions of WUS and WUS-related homeobox (WOX) transcription factors in diverse signaling pathways governing shoot meristem biology and several other aspects of plant dynamics. Transcription factors (TFs) are master regulators involved in controlling different cellular and biological functions as well as diverse signaling pathways in plant growth and development. WUSCHEL (WUS) is a homeodomain transcription factor necessary for the maintenance of the stem cell niche in the shoot apical meristem, the differentiation of lateral primordia, plant cell totipotency and other diverse cellular processes. Recent research about WUS has uncovered several unique features including the complex signaling pathways that further improve the understanding of vital network for meristem biology and crop productivity. In addition, several reports bridge the gap between WUS expression and plant signaling pathway by identifying different WUS and WUS-related homeobox (WOX) genes during the formation of shoot (apical and axillary) meristems, vegetative-to-embryo transition, genetic transformation, and other aspects of plant growth and development. In this respect, the WOX family of TFs comprises multiple members involved in diverse signaling pathways, but how these pathways are regulated remains to be elucidated. Here, we review the current status and recent discoveries on the functions of WUS and newly identified WOX family members in the regulatory network of various aspects of plant dynamics.

How aerobic organisms exploit inevitably generated but potentially dangerous reactive oxygen species (ROS) to benefit normal life is a fundamental biological question. Locally accumulated ROS have been reported to prime stem cell differentiation. However, the underlying molecular mechanism is unclear. Here, we reveal that developmentally produced H 2 O 2 in plant shoot apical meristem (SAM) triggers reversible protein phase separation of TERMINATING FLOWER (TMF), a transcription factor that times flowering transition in the tomato by repressing pre-maturation of SAM. Cysteine residues within TMF sense cellular redox to form disulfide bonds that concatenate multiple TMF molecules and elevate the amount of intrinsically disordered regions to drive phase separation. Oxidation triggered phase separation enables TMF to bind and sequester the promoter of a floral identity gene ANANTHA to repress its expression. The reversible transcriptional condensation via redox-regulated phase separation endows aerobic organisms with the flexibility of gene control in dealing with developmental cues. Plants utilize naturally produced ROS in shoot apical stem cells as a developmental signal to trigger phase separation of TMF. The resulting transcriptional condensates repress expression of the floral identity gene to precisely time flowering.

Zachary Lippman and colleagues report mutations in the tomato ortholog of CLV1 and a gene encoding a hydroxyproline O-arabinosyltransferase enzyme that modifies CLV3, both of which cause fasciated flowers and fruits owing to increased meristem size. They also find that a natural mutation in CLV3 was a major target of selection during tomato domestication. Shoot meristems of plants are composed of stem cells that are continuously replenished through a classical feedback circuit involving the homeobox WUSCHEL ( WUS ) gene and the CLAVATA ( CLV ) gene signaling pathway. In CLV signaling, the CLV1 receptor complex is bound by CLV3, a secreted peptide modified with sugars. However, the pathway responsible for modifying CLV3 and its relevance for CLV signaling are unknown. Here we show that tomato inflorescence branching mutants with extra flower and fruit organs due to enlarged meristems are defective in arabinosyltransferase genes. The most extreme mutant is disrupted in a hydroxyproline O-arabinosyltransferase and can be rescued with arabinosylated CLV3. Weaker mutants are defective in arabinosyltransferases that extend arabinose chains, indicating that CLV3 must be fully arabinosylated to maintain meristem size. Finally, we show that a mutation in CLV3 increased fruit size during domestication. Our findings uncover a new layer of complexity in the control of plant stem cell proliferation.

Meristems encompass stem/progenitor cells that sustain postembryonic growth of all plant organs. How meristems are activated and sustained by nutrient signalling remains enigmatic in photosynthetic plants. Combining chemical manipulations and chemical genetics at the photoautotrophic transition checkpoint, we reveal that shoot photosynthesis-derived glucose drives target-of-rapamycin (TOR) signalling relays through glycolysis and mitochondrial bioenergetics to control root meristem activation, which is decoupled from direct glucose sensing, growth-hormone signalling and stem-cell maintenance. Surprisingly, glucose–TOR signalling dictates transcriptional reprogramming of remarkable gene sets involved in central and secondary metabolism, cell cycle, transcription, signalling, transport and protein folding. Systems, cellular and genetic analyses uncover TOR phosphorylation of E2Fa transcription factor for an unconventional activation of S-phase genes, and glucose-signalling defects in e2fa root meristems. Our findings establish pivotal roles of glucose–TOR signalling in unprecedented transcriptional networks wiring central metabolism and biosynthesis for energy and biomass production, and integrating localized stem/progenitor-cell proliferation through inter-organ nutrient coordination to control developmental transition and growth. The authors show that photosynthetically derived glucose drives target-of-rapamycin signalling, resulting in transcriptional reprogramming of genes involved in cell cycle regulation. Nutrients' role in meristem activation Plant meristems contain stem cells that sustain postembryonic growth. Current models of meristem function focus on hormonal regulation, but here Jen Sheen and colleagues study the role of photosynthesis-driven nutrient signalling. They find that photosynthetically derived glucose drives TOR (target-of-rapamycin) signalling, resulting in transcriptional reprogramming of genes involved in cell cycle regulation. TOR directly activates E2Fa transcription factor, leading to cell cycle progression and root growth.

Plant organ size shows remarkable uniformity within species indicating strong endogenous control. We have identified a plant growth regulatory gene, functionally and structurally homologous to human EBP1. Plant EBP1 levels are tightly regulated; gene expression is highest in developing organs and correlates with genes involved in ribosome biogenesis and function. EBP1 protein is stabilised by auxin. Elevating or decreasing EBP1 levels in transgenic plants results in a dose‐dependent increase or reduction in organ growth, respectively. During early stages of organ development, EBP1 promotes cell proliferation, influences cell‐size threshold for division and shortens the period of meristematic activity. In postmitotic cells, it enhances cell expansion. EBP1 is required for expression of cell cycle genes; CyclinD3;1, ribonucleotide reductase 2 and the cyclin‐dependent kinase B1;1. The regulation of these genes by EBP1 is dose and auxin dependent and might rely on the effect of EBP1 to reduce RBR1 protein level. We argue that EBP1 is a conserved, dose‐dependent regulator of cell growth that is connected to meristematic competence and cell proliferation via regulation of RBR1 level.

Environmental cues profoundly modulate cell proliferation and cell elongation to inform and direct plant growth and development. External phosphate (Pi) limitation inhibits primary root growth in many plant species. However, the underlying Pi sensory mechanisms are unknown. Here we genetically uncouple two Pi sensing pathways in the root apex of Arabidopsis thaliana. First, the rapid inhibition of cell elongation in the transition zone is controlled by transcription factor STOP1, by its direct target, ALMT1, encoding a malate channel, and by ferroxidase LPR1, which together mediate Fe and peroxidase-dependent cell wall stiffening. Second, during the subsequent slow inhibition of cell proliferation in the apical meristem, which is mediated by LPR1-dependent, but largely STOP1–ALMT1-independent, Fe and callose accumulate in the stem cell niche, leading to meristem reduction. Our work uncovers STOP1 and ALMT1 as a signalling pathway of low Pi availability and exuded malate as an unexpected apoplastic inhibitor of root cell wall expansion.

The phytohormone salicylic acid (SA) is well known for its induction of pathogenesis-related proteins and systemic acquired resistance; SA also has specific effects on plant growth and development. Here we analyzed the effect of SA on Arabidopsis (Arabidopsis thaliana) root development. We show that exogenous SA treatment at low (below 50 𝜇M) and high (greater than 50 𝜇M) concentrations affect root meristem development in two different PR1-independent ways. Low-concentration SA promoted adventitious roots and altered architecture of the root apical meristem, whereas high-concentration SA inhibited all growth processes in the root. All exposures to exogenous SA led to changes in auxin synthesis and transport. A wide range of SA treatment concentrations activated auxin synthesis, but the effect of SA on auxin transport was dose dependent. Mathematical modeling of auxin synthesis and transport predicted auxin accumulation or depletion in the root tip following low- or high-concentration SA treatments, respectively. SA-induced auxin accumulation led to the formation of more layers of columella initials, an additional cortical cell layer (middle cortex), and extra files of epidermis, cortex, and endodermis cells. Suppression of SHORT ROOT and activation of CYCLIN D6;1 mediated the changes in radial architecture of the root. We propose that low-concentration SA plays an important role in shaping root meristem structure and root system architecture.

Complex multicellular organisms evolved on Earth in an oxygen-rich atmosphere 1 ; their tissues, including stem-cell niches, require continuous oxygen provision for efficient energy metabolism 2 . Notably, the maintenance of the pluripotent state of animal stem cells requires hypoxic conditions, whereas higher oxygen tension promotes cell differentiation 3 . Here we demonstrate, using a combination of genetic reporters and in vivo oxygen measurements, that plant shoot meristems develop embedded in a low-oxygen niche, and that hypoxic conditions are required to regulate the production of new leaves. We show that hypoxia localized to the shoot meristem inhibits the proteolysis of an N-degron-pathway 4 , 5 substrate known as LITTLE ZIPPER 2 (ZPR2)—which evolved to control the activity of the class-III homeodomain-leucine zipper transcription factors 6 – 8 —and thereby regulates the activity of shoot meristems. Our results reveal oxygen as a diffusible signal that is involved in the control of stem-cell activity in plants grown under aerobic conditions, which suggests that the spatially distinct distribution of oxygen affects plant development. In molecular terms, this signal is translated into transcriptional regulation by the N-degron pathway, thereby linking the control of metabolic activity to the regulation of development in plants. Hypoxia in the shoot meristem of Arabidopsis links the regulation of metabolic activity to development by inhibiting proteolysis of a substrate of the N-degron pathway, which controls class-III homeodomain-leucine zipper transcription factors.

In plants, roots are essential for water and nutrient acquisition. MicroRNAs (miRNAs) regulate their target mRNAs by transcript cleavage and/or inhibition of protein translation and are known as major post‐transcriptional regulators of various developmental pathways and stress responses. In Arabidopsis thaliana, four isoforms of miR169 are encoded by 14 different genes and target diverse mRNAs, encoding subunits A of the NF‐Y transcription factor complex. These miRNA isoforms and their targets have previously been linked to nutrient signalling in plants. By using mimicry constructs against different isoforms of miR169 and miR‐resistant versions of NF‐YA genes we analysed the role of specific miR169 isoforms in root growth and branching. We identified a regulatory node involving the particular miR169defg isoform and NF‐YA2 and NF‐YA10 genes that acts in the control of primary root growth. The specific expression of MIM169defg constructs altered specific cell type numbers and dimensions in the root meristem. Preventing miR169defg‐regulation of NF‐YA2 indirectly affected laterial root initiation. We also showed that the miR169defg isoform affects NF‐YA2 transcripts both at mRNA stability and translation levels. We propose that a specific miR169 isoform and the NF‐YA2 target control root architecture in Arabidopsis.