The instructive role of mechanical cues during morphogenesis is increasingly being recognized in all kingdoms. Patterns of mechanical stress depend on shape, growth and external factors. In plants, ...the cell wall integrates these three parameters to function as a hub for mechanical feedback. Plant cells are interconnected by cell walls that provide structural integrity and yet are flexible enough to act as both targets and transducers of mechanical cues. Such cues may act locally at the subcellular level or across entire tissues, requiring tight control of both cell-wall composition and cell–cell adhesion. Here we focus on how changes in cell-wall chemistry and mechanics act in communicating diverse cues to direct growth asymmetries required for plant morphogenesis. We explore the role of cellulose microfibrils, microtubule arrays and pectin methylesterification in the transduction of mechanical cues during morphogenesis. Plant hormones can affect the mechanochemical composition of the cell wall and, in turn, the cell wall can modulate hormone signaling pathways, as well as the tissue-level distribution of these hormones. This also leads us to revisit the position of biochemical growth factors, such as plant hormones, acting both upstream and downstream of mechanical signaling. Finally, while the structure of the cell wall is being elucidated with increasing precision, existing data clearly show that the integration of genetic, biochemical and theoretical studies will be essential for a better understanding of the role of the cell wall as a hub for the mechanical control of plant morphogenesis.
Jonsson et al. review how plant cell walls integrate mechanical cues to guide morphogenesis.
Stem cell populations in meristematic tissues at distinct locations in the plant body provide the potency of continuous plant growth. Primary meristems, at the apices of the plant body, contribute ...mainly to the elongation of the main plant axes, whereas secondary meristems in lateral positions are responsible for the thickening of these axes. The stem cells of the vascular cambium-a secondary lateral meristem-produce the secondary phloem (bast) and secondary xylem (wood). The sites of primary and secondary growth are spatially separated, and mobile signals are expected to coordinate growth rates between apical and lateral stem cell populations. Although the underlying mechanisms have not yet been uncovered, it seems likely that hormones, peptides, and mechanical cues orchestrate primary and secondary growth. In this review, we highlight the current knowledge and recent discoveries of how cambial stem cell activity is regulated, with a focus on mobile signals and the response of cambial activity to environmental and stress factors.
Trees growing in boreal and temperate regions synchronize their growth with seasonal climatic changes in adaptive responses that are essential for their survival. These trees cease growth before the ...winter and establish a dormant state during which growth cessation is maintained by repression of responses to growth-promotive signals. Reactivation of growth in the spring follows the release from dormancy promoted by prolonged exposure to low temperature during the winter. The timing of the key events and regulation of the molecular programs associated with the key stages of the annual growth cycle are controlled by two main environmental cues: photoperiod and temperature. Recently, key components mediating photoperiodic control of growth cessation and bud set have been identified, and striking similarities have been observed in signaling pathways controlling growth cessation in trees and floral transition in Arabidopsis. Although less well understood, the regulation of bud dormancy and bud burst may involve cell–cell communication and chromatin remodeling. Here, we discuss current knowledge of the molecular-level regulation of the annual growth cycle of woody trees in temperate and boreal regions, and identify key questions that need to be addressed in the future.
How plants adapt their developmental patterns to regular seasonal changes is an important question in biology. The annual growth cycle in perennial long-lived trees is yet another example of how ...plants can adapt to seasonal changes. The two main signals that plants rely on to respond to seasonal changes are photoperiod and temperature, and these signals have critical roles in the temporal regulation of the annual growth cycle of trees.
This review presents the latest findings to provide insight into the molecular mechanisms that underlie how photoperiodic and temperature signals regulate seasonal growth in trees.
The results point to a high level of conservation in the signalling pathways that mediate photoperiodic control of seasonal growth in trees and flowering in annual plants such as arabidopsis. Furthermore, the data indicate that symplastic communication may mediate certain aspects of seasonal growth. Although considerable insight into the control of phenology in model plants such as poplar and spruce has been obtained, the future challenge is extending these studies to other, non-model trees.
Perennials in boreal and temperate ecosystems display seasonally synchronized growth. In many tree species, prior to the advent of winter, exposure to photoperiods shorter than a critical threshold ...for growth (short days; SDs) induces growth cessation, culminating in the formation of an apical bud that encloses the shoot apical meristem and arrested leaf primordia 1–4. Following growth cessation, subsequent exposure to SDs induces transition to dormancy in the shoot apex 5. Establishment of dormancy is crucial for winter survival and is characterized by the inability of the shoot meristem to respond to growth-promotive signals 6. Recently, SDs were shown to induce bud dormancy by activating the abscisic acid (ABA) pathway. ABA upregulates expression of CALLOSE SYNTHASE 1 (CALS1) and suppresses glucanases that break down callose to induce the blockage of intracellular conduits (plasmodesmata; PDs) with callosic plugs called “dormancy sphincters” that by restricting access to growth-promotive signals promote dormancy 7. However, components downstream of ABA in dormancy regulation remain largely unknown, and thus there are significant gaps in our understanding of photoperiodic control of bud dormancy. Here we demonstrate that SVL, orthologous to Arabidopsis floral repressor SHORT VEGETATIVE PHASE (SVP), is a mediator of photoperiodic control of dormancy downstream of the ABA pathway in hybrid aspen. SVL downregulation impairs dormancy, whereas SVL overexpression suppresses dormancy defects resulting from ABA insensitivity. Downstream, SVL induces callose synthase expression and negatively regulates the gibberellic acid (GA) pathway to promote dormancy, thus revealing the regulatory module mediating photoperiodic control of dormancy by ABA.
•SHORT VEGETATIVE PHASE ortholog SVL mediates photoperiodic control of dormancy•SVL acts downstream of ABA in dormancy regulation•SVL promotes dormancy by suppressing the growth-promotive gibberellic acid pathway•SVL activates CALLOSE SYNTHASE expression, a key mediator of plasmodesmatal closure
Singh et al. have identified SHORT VEGETATIVE PHASE ortholog SVL as a key component in ABA-mediated photoperiodic control of bud dormancy. They show that SVL simultaneously suppresses the growth-promotive GA pathway and induces the expression of CALLOSE SYNTHASE 1 (CALS1), which mediates plasmodesmatal closure to promote dormancy.
Despite the crucial roles of phytohormones in plant development, comparison of the exact distribution profiles of different hormones within plant meristems has thus far remained scarce. Vascular ...cambium, a wide lateral meristem with an extensive developmental zonation, provides an optimal system for hormonal and genetic profiling. By taking advantage of this spatial resolution, we show here that two major phytohormones, cytokinin and auxin, display different yet partially overlapping distribution profiles across the cambium. In contrast to auxin, which has its highest concentration in the actively dividing cambial cells, cytokinins peak in the developing phloem tissue of a Populus trichocarpa stem. Gene expression patterns of cytokinin biosynthetic and signaling genes coincided with this hormonal gradient. To explore the functional significance of cytokinin signaling for cambial development, we engineered transgenic Populus tremula × tremuloides trees with an elevated cytokinin biosynthesis level. Confirming that cytokinins function as major regulators of cambial activity, these trees displayed stimulated cambial cell division activity resulting in dramatically increased (up to 80% in dry weight) production of the lignocellulosic trunk biomass. To connect the increased growth to hormonal status, we analyzed the hormone distribution and genome-wide gene expression profiles in unprecedentedly high resolution across the cambial zone. Interestingly, in addition to showing an elevated cambial cytokinin content and signaling level, the cambial auxin concentration and auxin-responsive gene expression were also increased in the transgenic trees. Our results indicate that cytokinin signaling specifies meristematic activity through a graded distribution that influences the amplitude of the cambial auxin gradient.
•Gene expression was profiled globally across the cambium in high resolution•Auxin and cytokinin display distinct distribution profiles across the cambium•Increased cytokinin content and signaling level stimulate cambial cell divisions•Elevation of cytokinin content leads to an increased cambial auxin concentration
A new report explores how two major phytohormones, cytokinin and auxin, contribute to the control of tree trunk growth. Immanen et al. show that by boosting cytokinin biosynthesis, they can both increase auxin level and stimulate lignocellulosic biomass production. Both hormones represent optimal targets for tree breeding and forest biotechnology.
Perennial trees have the amazing ability to adjust their growth rate to both adverse and favorable seasonally reoccurring environmental conditions over hundreds of years. In trunks and stems, the ...basis for the tuning of seasonal growth rate is the regulation of cambial stem cell activity. Cambial stem cell quiescence and dormancy protect the tree from potential physiological and genomic damage caused by adverse growing conditions and may permit a long lifespan. Cambial dormancy and longevity are both aspects of a tree’s life for which the study of cambial stem cell behavior in the annual model plant Arabidopsis is inadequate. Recent functional analyses of hormone perception and catabolism mutants in Populus indicate that shoot-derived long-range signals, as well as local cues, steer cambial activity. Auxin is central to the regulation of cambial activity and probably also maintenance. Emerging genome editing and phenotyping technologies will enable the identification of down-stream targets of hormonal action and facilitate the genetic dissection of complex traits of cambial biology.
Tissue bending is vital to plant development, as exemplified by apical hook formation during seedling emergence by bending of the hypocotyl. How tissue bending is coordinated during development ...remains poorly understood, especially in plants where cells are attached via rigid cell walls. Asymmetric distribution of the plant hormone auxin underlies differential cell elongation during apical hook formation. Yet the underlying mechanism remains unclear. Here, we demonstrate spatial correlation between asymmetric auxin distribution, methylesterified homogalacturonan (HG) pectin, and mechanical properties of the epidermal layer of the hypocotyl in Arabidopsis. Genetic and cell biological approaches show that this mechanochemical asymmetry is essential for differential cell elongation. We show that asymmetric auxin distribution underlies differential HG methylesterification, and conversely changes in HG methylesterification impact the auxin response domain. Our results suggest that a positive feedback loop between auxin distribution and HG methylesterification underpins asymmetric cell wall mechanochemical properties to promote tissue bending and seedling emergence.
Display omitted
•Asymmetric pectin methylesterification is required for differential growth•Auxin distribution regulates pectin methylesterification during differential growth•Feedback between pectin and auxin via PIN proteins facilitates growth asymmetry
Using hook development as model in Arabidopsis, Jonsson et al. demonstrate a mechanochemical feedback between the plant hormone auxin and pectin methylesterification regulates differential cell elongation to facilitate tissue bending essential for seedling emergence from soil.
Photoperiodic control of development plays a key role in adaptation of plants to seasonal changes. A signaling module consisting of CONSTANS (CO) and FLOWERING LOCUS T (FT) mediates in photoperiodic ...control of a variety of developmental transitions (e.g., flowering, tuberization, and seasonal growth cessation in trees). How this conserved CO/FT module can mediate in the photoperiodic control of diverse unrelated developmental programs is poorly understood.
We show that Like-AP1 (LAP1), a tree ortholog of Arabidopsis floral meristem identity gene APETALA1 (AP1), mediates in photoperiodic control of seasonal growth cessation downstream of the CO/FT module in hybrid aspen. Using LAP1 overexpressors and RNAi-suppressed transgenic trees, we demonstrate that short day (SD)-mediated downregulation of LAP1 expression is required for growth cessation. In contrast with AP1 targets in flowering, LAP1 acts on AINTEGUMENTA-like 1 transcription factor, which is implicated in SD-mediated growth cessation. Intriguingly, unlike AP1 in Arabidopsis, ectopic expression of LAP1 fails to induce early flowering in hybrid aspen trees.
These results indicate that AP1 ortholog in trees has acquired a novel function in photoperiodic regulation of seasonal growth. Thus, photoperiodic signaling pathway may have diverged downstream of AP1/LAP1 rather than the CO/FT module during evolution. Moreover, control of flowering by the CO/FT module can be uncoupled from its role in photoperiodic control of seasonal growth in trees. Thus, our findings can explain mechanistically how a conserved signaling module can mediate in the control of a highly diverse set of developmental transitions by a similar input signal, namely photoperiod.
•AP1 ortholog LAP1 mediates in photoperiodic control of growth in trees•LAP1 acts downstream of the CO/FT module•LAP1 mediates in control of cell-proliferation regulator AINTEGUMENTA-like 1
Photoperiod controls flowering, tuberization, and seasonal growth in plants. Azeez et al. show that LAP1, a tree ortholog of Arabidopsis floral meristem identity AP1, mediates in photoperiodic control of seasonal growth in trees. LAP1 acts downstream of the CO/FT module and controls the expression of cell-cycle regulator AINTEGUMENTA-like 1.
PDF
