An Update on the Signals Controlling Shoot Branching.

Plant hormones known as strigolactones control plant development and interactions between host plants and symbiotic fungi or parasitic weeds1–4. In Arabidopsis thaliana and rice, the proteins DWARF14 (D14), MORE AXILLARY GROWTH 2 (MAX2), SUPPRESSOR OF MAX2-LIKE 6, 7 and 8 (SMXL6, SMXL7 and SMXL8) and their orthologues form a complex upon strigolactone perception and play a central part in strigolactone signalling5–10. However, whether and how strigolactones activate downstream transcription remains largely unknown. Here we use a synthetic strigolactone to identify 401 strigolactone-responsive genes in Arabidopsis, and show that these plant hormones regulate shoot branching, leaf shape and anthocyanin accumulation mainly through transcriptional activation of the BRANCHED 1, TCP DOMAIN PROTEIN 1 and PRODUCTION OF ANTHOCYANIN PIGMENT 1 genes. We find that SMXL6 targets 729 genes in the Arabidopsis genome and represses the transcription of SMXL6, SMXL7 and SMXL8 by binding directly to their promoters, showing that SMXL6 serves as an autoregulated transcription factor to maintain the homeostasis of strigolactone signalling. These findings reveal an unanticipated mechanism through which a transcriptional repressor of hormone signalling can directly recognize DNA and regulate transcription in higher plants. Many of the molecular targets of strigolactones—plant hormones involved in development and in interactions with symbiotic and parasitic organisms—are uncovered, revealing how strigolactones function and an intriguing role for self-regulation of a downstream transcription factor.

Transcriptional regulation of strigolactone signalling in Arabidopsis

In boreal and temperate ecosystems, temperature signal regulates the reactivation of growth (bud break) in perennials in the spring. Molecular basis of temperature-mediated control of bud break is poorly understood. Here we identify a genetic network mediating the control of bud break in hybrid aspen. The key components of this network are transcription factor SHORT VEGETATIVE PHASE-LIKE (SVL), closely related to Arabidopsis floral repressor SHORT VEGETATIVE PHASE, and its downstream target TCP18, a tree homolog of a branching regulator in Arabidopsis. SVL and TCP18 are downregulated by low temperature. Genetic evidence demonstrates their role as negative regulators of bud break. SVL mediates bud break by antagonistically acting on gibberellic acid (GA) and abscisic acid (ABA) pathways, which function as positive and negative regulators of bud break, respectively. Thus, our results reveal the mechanistic basis for temperature-cued seasonal control of a key phenological event in perennial plants.

/pdf/a-genetic-network-mediating-the-control-of-bud-break-in-5g2hwy09dk.pdf

A genetic network mediating the control of bud break in hybrid aspen.

Floret fertility is a key determinant of the number of grains per inflorescence in cereals. During the evolution of wheat (Triticum sp.), floret fertility has increased, such that current bread wheat (Triticum aestivum) cultivars set three to five grains per spikelet. However, little is known regarding the genetic basis of floret fertility. The locus Grain Number Increase 1 (GNI1) is shown here to be an important contributor to floret fertility. GNI1 evolved in the Triticeae through gene duplication. The gene, which encodes a homeodomain leucine zipper class I (HD-Zip I) transcription factor, was expressed most abundantly in the most apical floret primordia and in parts of the rachilla, suggesting that it acts to inhibit rachilla growth and development. The level of GNI1 expression has decreased over the course of wheat evolution under domestication, leading to the production of spikes bearing more fertile florets and setting more grains per spikelet. Genetic analysis has revealed that the reduced-function allele GNI-A1 contributes to the increased number of fertile florets per spikelet. The RNAi-based knockdown of GNI1 led to an increase in the number of both fertile florets and grains in hexaploid wheat. Mutants carrying an impaired GNI-A1 allele out-yielded WT allele carriers under field conditions. The data show that gene duplication generated evolutionary novelty affecting floret fertility while mutations favoring increased grain production have been under selection during wheat evolution under domestication.

https://www.pnas.org/content/pnas/116/11/5182.full.pdf

Unleashing floret fertility in wheat through the mutation of a homeobox gene

For perennial plants, bud dormancy is a crucial step as its progression over winter determines the quality of bud break, flowering, and fruiting. In the past decades, many studies, based on metabolic, physiological, subcellular, genetic, and genomic analyses, have unraveled mechanisms underlying bud dormancy progression. Overall, all the pathways identified are interconnected in a very complex manner. Here, we review early and recent findings on the dormancy processes in buds of temperate fruit trees species including hormonal signaling, the role of plasma membrane, carbohydrate metabolism, mitochondrial respiration and oxidative stress, with an effort to link them together and emphasize the central role of reactive oxygen species accumulation in the control of dormancy progression.

/pdf/bud-dormancy-in-perennial-fruit-tree-species-a-pivotal-role-zvcq9nixit.pdf

Bud Dormancy in Perennial Fruit Tree Species: A Pivotal Role for Oxidative Cues.

Shoot-branching patterns determine key aspects of plant life and are important targets for crop breeding. However, we are still largely ignorant of the genetic networks controlling locally the most important decision during branch development: whether the axillary bud, or branch primordium, grows out to give a lateral shoot or remains dormant. Here we show that, inside the buds, the TEOSINTE BRANCHED1, CYCLOIDEA, PCF (TCP) transcription factor BRANCHED1 (BRC1) binds to and positively regulates the transcription of three related Homeodomain leucine zipper protein (HD-ZIP)-encoding genes: HOMEOBOX PROTEIN 21 (HB21), HOMEOBOX PROTEIN 40 (HB40), and HOMEOBOX PROTEIN 53 (HB53). These three genes, together with BRC1, enhance 9-CIS-EPOXICAROTENOID DIOXIGENASE 3 (NCED3) expression, lead to abscisic acid accumulation, and trigger hormone response, thus causing suppression of bud development. This TCP/HD-ZIP genetic module seems to be conserved in dicot and monocotyledonous species to prevent branching under light-limiting conditions.

https://www.pnas.org/content/pnas/114/2/E245.full.pdf

Abscisic acid signaling is controlled by a BRANCHED1/HD-ZIP I cascade in Arabidopsis axillary buds.

Plant shoot systems give rise to characteristic above-ground plant architectures Shoots are formed from axillary meristems and buds, whose growth and development is modulated by systemic and local signals These cues convey information about nutrient and water availability, light quality, sink/source organ activity and other variables that determine the timeliness and competence to maintain development of new shoots This information is translated into a local response, in meristems and buds, of growth or quiescence Although some key genes involved in the onset of bud latency have been identified, the gene regulatory networks (GRNs) controlled by these genes are not well defined Moreover, it has not been determined whether bud dormancy induced by environmental cues, such as a low red-to-far-red light ratio, shares genetic mechanisms with bud latency induced by other causes, such as apical dominance or a short-day photoperiod Furthermore, the evolution and conservation of these GRNs throughout angiosperms is not well established We have reanalyzed public transcriptomic datasets that compare quiescent and active axillary buds of Arabidopsis, with datasets of axillary buds of the woody species Vitis vinifera (grapevine) and apical buds of Populus tremula x Populus alba (poplar) during the bud growth-to-dormancy transition Our aim was to identify potentially common GRNs induced during the process that leads to bud para-, eco- and endodormancy In Arabidopsis buds that are entering eco- or paradormancy, we have identified four induced interrelated GRNs that correspond to a carbon (C) starvation syndrome, typical of tissues undergoing C depletion This response is also detectable in poplar and grapevine buds before and during the transition to dormancy In all eukaryotes, C limiting conditions are coupled to growth arrest and latency like that observed in dormant axillary buds Bud dormancy might thus be partly a consequence of the underlying C starvation syndrome triggered by environmental and endogenous cues that anticipate or signal conditions unfavorable for sustained shoot growth

/pdf/a-conserved-carbon-starvation-response-underlies-bud-4iipc3wa61.pdf

A Conserved Carbon Starvation Response Underlies Bud Dormancy in Woody and Herbaceous Species.

To grow or not to grow, a power-saving program induced in dormant buds.

The control of branch outgrowth is critical for plant fitness, stress resilience and crop yield. The Arabidopsis thaliana transcription factor BRANCHED1 (BRC1) plays a pivotal role in this process as it integrates signals that inhibit axillary bud growth to control shoot branching. Despite the remarkable activity of BRC1 as a potent growth inhibitor, the mechanisms by which it promotes and maintains bud dormancy are still largely unknown. 
Here we combine ChIP-seq, transcriptomic and systems biology approaches to characterise the BRC1-regulated gene network. We identify a group of BRC1 direct target genes encoding transcription factors (BTFs) that orchestrate, together with BRC1, an intricate transcriptional network enriched in abscisic acid signalling components. The BRC1 network is enriched in feed-forward loops and feedback loops, robust against noise and mutation, reversible in response to stimuli, and stable once established. This knowledge is fundamental to adapt plant architecture and crop production to ever-changing environmental conditions.

Carlos Tarancón

Papers

Abscisic acid signaling is controlled by a BRANCHED1/HD-ZIP I cascade in Arabidopsis axillary buds.

A Conserved Carbon Starvation Response Underlies Bud Dormancy in Woody and Herbaceous Species.

To grow or not to grow, a power-saving program induced in dormant buds.

A gene regulatory network critical for axillary bud dormancy directly controlled by Arabidopsis BRANCHED1