Complexity of SMAX1 signaling during seedling establishment

Karrikins (KARs) are small butenolide compounds identified in the smoke of burning vegetation. Along with the stimulating effects on seed germination, KARs also regulate seedling vigor and adaptive behaviors, such as seedling morphogenesis, root hair development, and stress acclimation. The pivotal KAR signaling repressor, SUPPRESSOR OF MAX2 1 (SMAX1), plays central roles in these developmental and morphogenic processes through an extensive signaling network that governs seedling responses to endogenous and environmental cues. Here, we summarize the versatile roles of SMAX1 reported in recent years and discuss how SMAX1 integrates multiple growth hormone signals into optimizing seedling establishment. We also discuss the evolutionary relevance of the SMAX1-mediated signaling pathways during the colonization of aqueous plants to terrestrial environments.     

Of light and length: regulation of hypocotyl growth in Arabidopsis

At all stages, plant development results from a complex integration of multiple endogenous and environmental signals. The sedentary nature of plants strongly enhances the impact of the environment on plant development as compared to animal development. The embryonic and postembryonic seedling stem, called the hypocotyl, of the model species Arabidopsis (thale cress) has proved to be an excellent system for studying such signal interplay in the regulation of growth and developmental responses. The extension of the hypocotyl, which is regulated by a network of interacting factors, including light and plant hormones, is such a process. These regulatory factors often reciprocally regulate their biosynthesis and/or signalling. Here we present the current state of knowledge about the regulation of hypocotyl growth by a large repertoire of internal and external cues.     

Integrating hormone signaling and patterning mechanisms in plant development

Plant growth and development are driven by the bustling integration of a vast number of signals, among which plant hormones dominate. Understanding the role of hormones in particular developmental events requires their integration with developmental regulators known to be specific to those events. Using the increasing number of tools that can be utilized to probe hormone biosynthesis, transport and response, several recent studies have taken such an integrative approach, and in so doing have contributed to a clearer picture of precisely how hormones control plant development.     

One for All and All for One: Cross-Talk of Multiple Signals Controlling the Plant Phenotype

The plant hormone ethylene plays a pivotal role in steering various processes by regulating the biosynthesis, distribution, or signal transduction of other hormones. Ethylene also mediates the effects of other hormones. Similarly, hormones control the ethylene synthesis and signalling pathway. Eventually, integration of this network of signals leads to an appropriate morphological or biochemical response. Consequently, this cross-talk results in the characteristic plasticity associated with plant development. Here, the interplay of ethylene with other hormones is described for germination and seedling growth, stomatal control, and tissue elongation. The mechanisms by which this occurs are discussed in more detail.     

Hormone interactions at the root apical meristem

Plants exhibit an amazing developmental flexibility. Plant embryogenesis results in the establishment of a simple apical-basal axis represented by apical shoot and basal root meristems. Later, during postembryonic growth, shaping of the plant body continues by the formation and activation of numerous adjacent meristems that give rise to lateral shoot branches, leaves, flowers, or lateral roots. This developmental plasticity reflects an important feature of the plant's life strategy based on the rapid reaction to different environmental stimuli, such as temperature fluctuations, availability of nutrients, light or water and response resulting in modulation of developmental programs. Plant hormones are important endogenous factors for the integration of these environmental inputs and regulation of plant development. After a period of studies focused primarily on single hormonal pathways that enabled us to understand the hormone perception and signal transduction mechanisms, it became obvious that the developmental output mediated by a single hormonal pathway is largely modified through a whole network of interactions with other hormonal pathways. In this review, we will summarize recent knowledge on hormonal networks that regulate the development and growth of root with focus on the hormonal interactions that shape the root apical meristem.     

Plant Development: Should I Stop or Should I Grow?

Plant growth is tightly controlled through the integration of environmental cues with the physiological status of the seedling. A recent study now proposes a model explaining how the plant hormone ethylene triggers opposite growth responses depending on the light environment.     

Hormonal input in plant meristems: A balancing act

Plant hormones are a group of chemically diverse molecules that control virtually all aspects of plant development. Classical plant hormones were identified many decades ago in physiology studies that addressed plant growth regulation. In recent years, biochemical and genetic approaches led to the identification of many molecular components that mediate hormone activity, such as hormone receptors and hormone-regulated genes. This has greatly contributed to the understanding of the mechanisms underlying hormone activity and highlighted the intricate crosstalk and integration of hormone signalling and developmental pathways. Here we review and discuss recent findings on how hormones regulate the activity of shoot and root apical meristems.     

You're perfect, now change--redefining the role of developmental plasticity

The receptive field properties of neurons in the developing brain can in many cases be remarkably similar to those of adult neurons. This raises the question of why these same neurons need the capacity for such impressive developmental plasticity, most clearly demonstrated by the rewiring that occurs in response to sensory deprivation. The roles of developmental neuronal plasticity in the assimilation of neurons into a larger network, including temporal and cross-modal integration, are discussed.     

Signaling role of fructose mediated by FINS1/FBP in Arabidopsis thaliana

Sugars are evolutionarily conserved signaling molecules that regulate the growth and development of both unicellular and multicellular organisms. As sugar-producing photosynthetic organisms, plants utilize glucose as one of their major signaling molecules. However, the details of other sugar signaling molecules and their regulatory factors have remained elusive, due to the complexity of the metabolite and hormone interactions that control physiological and developmental programs in plants. We combined information from a gain-of-function cell-based screen and a loss-of-function reverse-genetic analysis to demonstrate that fructose acts as a signaling molecule in Arabidopsis thaliana. Fructose signaling induced seedling developmental arrest and interacted with plant stress hormone signaling in a manner similar to that of glucose. For fructose signaling responses, the plant glucose sensor HEXOKINASE1 (HXK1) was dispensable, while FRUCTOSE INSENSITIVE1 (FINS1), a putative FRUCTOSE-1,6-BISPHOSPHATASE, played a crucial role. Interestingly, FINS1 function in fructose signaling appeared to be independent of its catalytic activity in sugar metabolism. Genetic analysis further indicated that FINS1-dependent fructose signaling may act downstream of the abscisic acid pathway, in spite of the fact that HXK1-dependent glucose signaling works upstream of hormone synthesis. Our findings revealed that multiple layers of controls by fructose, glucose, and abscisic acid finely tune the plant autotrophic transition and modulate early seedling establishment after seed germination.     

ADAPTIVE RADIATIONS,ECOLOGICAL SPECIALIZATION,AND THE EVOLUTIONARY INTEGRATION OF COMPLEX MORPHOLOGICAL STRUCTURES

The evolutionary integration of complex morphological structures is a macroevolutionary pattern in which morphogenetic components evolve in a coordinated fashion, which can result from the interplay among processes of developmental, genetic integration, and different types of selection. We tested hypotheses of ecological versus developmental factors underlying patterns of within‐species and evolutionary integration in the mandible of phyllostomid bats, during the most impressive ecological and morphological radiation among mammals. Shape variation of mandibular morphogenetic components was associated with diet, and the transition of integration patterns from developmental to within‐species to evolutionary was examined. Within‐species (as a proxy to genetic) integration in different lineages resembled developmental integration regardless of diet specialization, however, evolutionary integration patterns reflected selection in different mandibular components. For dietary specializations requiring extensive functional changes in mastication patterns or biting, such as frugivores and sanguivores, the evolutionary integration pattern was not associated with expected within‐species or developmental integration. On the other hand, specializations with lower mastication demands or without major functional reorganization (such as nectarivores and carnivores), presented evolutionary integration patterns similar to the expected developmental pattern. These results show that evolutionary integration patterns are largely a result of independent selection on specific components regardless of developmental modules.     

Branching of the PIF3 regulatory network in Arabidopsis: Roles of PIF3-regulated MIDAs in seedling development in the dark and in response to light

Plants need to accurately adjust their development after germination in the underground darkness to ensure survival of the seedling, both in the dark and in the light upon reaching the soil surface. Recent studies have established that the photoreceptors phytochromes and the bHLH phytochrome interacting factors PIFs regulate seedling development to adjust it to the prevailing light environment during post-germinative growth. However, complete understanding of the downstream regulatory network implementing these developmental responses is still lacking. In a recent work, published in The Plant Cell, we report a subset of PIF3-regulated genes in dark-grown seedlings that we have named MIDAs (MISREGULATED IN DARK). Analysis of their functional relevance using mutants showed that four of them present phenotypic alterations in the dark, and that each affected a particular facet of seedling development, suggesting organ-specific branching in the signal that PIF3 relays downstream. Furthermore, our results also showed an altered response to light in seedlings with an impaired PIF3/MIDA regulatory network, indicating that these factors might also be essential to initiate and optimize the developmental adjustment of the seedling to the light environment.     

Hormonal pleiotropy and the juvenile hormone regulation of Drosophila development and life history

Understanding how traits are integrated at the organismal level remains a fundamental problem at the interface of developmental and evolutionary biology. Hormones, regulatory signaling molecules that coordinate multiple developmental and physiological processes, are major determinants underlying phenotypic integration. The probably best example for this is the lipid-like juvenile hormone (JH) in insects. Here we review the manifold effects of JH, the most versatile animal hormone, with an emphasis on the fruit fly Drosophila melanogaster, an organism amenable to both genetics and endocrinology. JH affects a remarkable number of processes and traits in Drosophila development and life history, including metamorphosis, behavior, reproduction, diapause, stress resistance and aging. While many molecular details underlying JH signaling remain unknown, we argue that studying "hormonal pleiotropy" offers intriguing insights into phenotypic integration and the mechanisms underlying life history evolution. In particular, we illustrate the role of JH as a key mediator of life history trade-offs.     

The highs and lows of plant life: temperature and light interactions in development

Plants must constantly respond to changes in the environment whilst maintaining developmental and growth processes if they are to survive into the next generation. A complex network of signals from temperature and light must correctly converge to achieve successful development, through vegetative to reproductive growth. Temperature can be thought of as an environmental factor that provides both 'inductive' and 'maintenance' signals in development. It can stimulate developmental processes such as seed dormancy release, germination and vernalization. However, when temperature is not regarded as inductive, an accommodating network of genes work in concert to ensure growth responses occur regardless of fluctuating microclimate conditions. Many of the temperature-regulated developmental pathways are intimately linked with light signaling. For example, light-temperature interactions are major determinants in the timing of reproductive development. Indeed, the ability to process and react to complex environmental cues is crucial for both normal and adaptive development in a changing environment. These responses are frequently mediated by manipulating the phytohormone network, which serves as a powerful, yet adaptable controller of development. This paper illustrates the influential role temperature perception plays throughout plant development and the close interaction between temperature, light and hormone signaling.     

CHRK1, a chitinase-related receptor-like kinase,plays a role in plant development and cytokinin homeostasis in tobacco

CHRK1 encodes a receptor-like kinase that contains a chitinase-related sequence in the extracellular domain in Nicotiana tabacum. In this study, we showed that CHRK1 is mainly expressed in the shoot apex region including leaf primordia and young leaves, and germinating seedlings and vascular tissues, based on GUS activity of transgenic tobacco plants carrying the CHRK1 promoter-GUS fusion gene. Transgenic tobacco plants in which CHRK1 expression was suppressed exhibited pleiotrophic developmental abnormality, including formation of proliferating shooty calli from emerging seedlings and severely altered seedling development. At the cellular level, ectopic cell proliferation, reduced cell specificity, and aberrant chloroplast development were observed. The transgenic lines contained 3-fold higher level of cytokinin than the wild-type plants. Consistently, the transgenic seedlings exhibited a typical cytokinin response in the absence of hormone, such as deetiolation under the dark. Based on these results, we propose that CHRK1 is involved in a developmental signaling pathway regulating cell proliferation/differentiation and the endogenous cytokinin levels in tobacco.     

Phytochrome coordinates Arabidopsis shoot and root development

The phytochrome family of photoreceptors are potent regulators of plant development, affecting a broad range of responses throughout the plant life cycle, including hypocotyl elongation, leaf expansion and apical dominance. The plant hormone auxin has previously been linked to these phytochrome-mediated responses; however, these studies have not identified the molecular mechanisms that underpin such extensive phytochrome and auxin cross-talk. In this paper, we show that phytochrome regulates the emergence of lateral roots, at least partly by manipulating auxin distribution within the seedling. Thus, shoot-localized phytochrome is able to act over long distances, through manipulation of auxin, to regulate root development. This work reveals an important role for phytochrome as a coordinator of shoot and root development, and provides insights into how phytochrome is able to exert such a powerful effect on growth and development. This new link between phytochrome and auxin may go some way to explain the extensive overlap in responses mediated by these two developmental regulators.     

Hormone signalling from a developmental context

The influence of hormones on plant growth and development has been clearly documented over the past 50 years. Now, with molecular genetics, the genes that convert changes in hormone levels into a cellular response are beginning to be identified. However, recent studies have demonstrated that the developmental context in which the hormones act plays a large influence on their synthesis and action. In this review, examples are given where known hormone response genes have been shown to have broader developmental roles as well as examples where genes that regulate developmental decisions, such as differentiation and fate, also influence hormone metabolism. The early conclusion of these studies is that an understanding of hormone signal transduction cannot be achieved in the absence of a developmental framework.     

ABA and sugar interactions regulating development: cross-talk or voices in a crowd?

Plant growth and development are controlled by the concerted action of many signaling pathways that integrate information from environmental signals with that from developmental and metabolic cues. Physiological studies have demonstrated that abscisic acid and sugars have both similar and antagonistic effects on diverse processes, including seed development, germination, and seedling growth. Recent genetic studies have identified several loci that are involved in both sugar and hormonal responses. It is rarely clear whether these apparent linkages reflect direct or indirect interactions between sugar and hormone signaling pathways, but the identification of gene products that are encoded at these loci is allowing these possibilities to be tested.     

Juvenile hormone mediates developmental integration between exaggerated traits and supportive traits in the horned flour beetle Gnatocerus cornutus

Sexually selected exaggerated traits are often coupled with modifications in other nontarget traits. In insects with weapons, enlargements of nontarget characters that functionally support the weapon often occur (i.e. supportive traits). The support of sexual traits requires developmental coordination among functionally related multiple traits—an explicit example of morphological integration. The genetic theory predicts that developmental integration among different body modules, for which development is regulated via different sets of genes, is likely to be coordinated by pleiotropic factors. However, the developmental backgrounds of morphological integrations are largely unknown. We tested the hypothesis that the juvenile hormone (JH), as a pleiotropic factor, mediates the integration between exaggerated and supportive traits in an armed beetle Gnatocerus cornutus. During combat, males of this beetle use exaggerated mandibles to lift up their opponents with the supportive traits, that is, the head and prothoracic body parts. Application of methoprene, a JH analog (JHA), during the larval to prepupal period, induced the formation of large mandibles relative to the body sizes in males. Morphometric examination of nontarget traits elucidated an increase in the relative sizes of supportive traits, including the head and prothoracic body parts. In addition, reductions in the hind wing area and elytra length, which correspond to flight and reproductive abilities, were detected. Our findings are consistent with the genetic theory and support the idea that JH is a key pleiotropic factor that coordinates the developmental integration of exaggerated traits and supportive characters, as well as resource allocation trade‐offs.