skip to main content


Title: Light Modulates Ethylene Synthesis, Signaling, and Downstream Transcriptional Networks to Control Plant Development
The inhibition of hypocotyl elongation by ethylene in dark-grown seedlings was the basis of elegant screens that identified ethylene-insensitive Arabidopsis mutants, which remained tall even when treated with high concentrations of ethylene. This simple approach proved invaluable for identification and molecular characterization of major players in the ethylene signaling and response pathway, including receptors and downstream signaling proteins, as well as transcription factors that mediate the extensive transcriptional remodeling observed in response to elevated ethylene. However, the dark-adapted early developmental stage used in these experiments represents only a small segment of a plant’s life cycle. After a seedling’s emergence from the soil, light signaling pathways elicit a switch in developmental programming and the hormonal circuitry that controls it. Accordingly, ethylene levels and responses diverge under these different environmental conditions. In this review, we compare and contrast ethylene synthesis, perception, and response in light and dark contexts, including the molecular mechanisms linking light responses to ethylene biology. One powerful method to identify similarities and differences in these important regulatory processes is through comparison of transcriptomic datasets resulting from manipulation of ethylene levels or signaling under varying light conditions. We performed a meta-analysis of multiple transcriptomic datasets to uncover transcriptional responses to ethylene that are both light-dependent and light-independent. We identified a core set of 139 transcripts with robust and consistent responses to elevated ethylene across three root-specific datasets. This “gold standard” group of ethylene-regulated transcripts includes mRNAs encoding numerous proteins that function in ethylene signaling and synthesis, but also reveals a number of previously uncharacterized gene products that may contribute to ethylene response phenotypes. Understanding these light-dependent differences in ethylene signaling and synthesis will provide greater insight into the roles of ethylene in growth and development across the entire plant life cycle.  more » « less
Award ID(s):
1817286
NSF-PAR ID:
10319874
Author(s) / Creator(s):
; ; ; ;
Date Published:
Journal Name:
Frontiers of plant science
Volume:
10
Issue:
1094
ISSN:
0016-2167
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Sigma factor (SIG) proteins contribute to promoter specificity of the plastid‐encodedRNApolymerase during chloroplast genome transcription. All six members of theSIGfamily, that is,SIG1–SIG6, are nuclear‐encoded proteins targeted to chloroplasts. Sigma factor 2 (SIG2) is a phytochrome‐regulated protein important for stoichiometric control of the expression of plastid‐ and nuclear‐encoded genes that impact plastid development and plant growth and development. AmongSIGfactors,SIG2 is required not only for transcription of chloroplast genes (i.e., anterograde signaling), but also impacts nuclear‐encoded, photosynthesis‐related, and light signaling‐related genes (i.e., retrograde signaling) in response to plastid functional status. AlthoughSIG2 is involved in photomorphogenesis in Arabidopsis, the molecular bases for its role in light signaling that impacts photomorphogenesis and aspects of photosynthesis have only recently begun to be investigated. Previously, we reported thatSIG2 is necessary for phytochrome‐mediated photomorphogenesis specifically under red (R) and far‐red light, thereby suggesting a link between phytochromes and nuclear‐encodedSIG2 in light signaling. To explore transcriptional roles ofSIG2 in R‐dependent growth and development, we performedRNAsequencing analysis to compare gene expression insig2‐2mutant and Col‐0 wild‐type seedlings at two developmental stages (1‐ and 7‐day). We identified a subset of misregulated genes involved in growth, hormonal cross talk, stress responses, and photosynthesis. To investigate the functional relevance of these gene expression analyses, we performed several comparative phenotyping tests. In these analyses, strongsig2mutants showed insensitivity to bioactiveGA3, high intracellular levels of hydrogen peroxide (H2O2) indicative of a stress response, and specific defects in photosynthesis, including elevated levels of cyclic electron flow (CEF) and nonphotochemical quenching (NPQ). We demonstrated thatSIG2 regulates a broader range of physiological responses at the molecular level than previously reported, with specific roles in red‐light‐mediated photomorphogenesis.

     
    more » « less
  2. Abstract Background

    Sexual-size dimorphism (SSD) is replete among animals, but while the selective pressures that drive the evolution of SSD have been well studied, the developmental mechanisms upon which these pressures act are poorly understood. Ours and others’ research has shown that SSD inD. melanogasterreflects elevated levels of nutritional plasticity in females versus males, such that SSD increases with dietary intake and body size, a phenomenon called sex-specific plasticity (SSP). Additional data indicate that while body size in both sexes responds to variation in protein level, only female body size is sensitive to variation in carbohydrate level. Here, we explore whether these difference in sensitivity at the morphological level are reflected by differences in how the insulin/IGF-signaling (IIS) and TOR-signaling pathways respond to changes in carbohydrates and proteins in females versus males, using a nutritional geometry approach.

    Results

    The IIS-regulated transcripts of4E-BPandInRmost strongly correlated with body size in females and males, respectively, but neither responded to carbohydrate level and so could not explain the sex-specific response to body size to dietary carbohydrate. Transcripts regulated by TOR-signaling did, however, respond to dietary carbohydrate in a sex-specific manner. In females, expression ofdILP5positively correlated with body size, while expression ofdILP2,3and8,was elevated on diets with a low concentration of both carbohydrate and protein. In contrast, we detected lower levels of dILP2 and 5 protein in the brains of females fed on low concentration diets. We could not detect any effect of diet ondILPexpression in males.

    Conclusion

    Although females and males show sex-specific transcriptional responses to changes in protein and carbohydrate, the patterns of expression do not support a simple model of the regulation of body-size SSP by either insulin- or TOR-signaling. The data also indicate a complex relationship between carbohydrate and protein level,dILPexpression and dILP peptide levels in the brain. In general, diet quality and sex both affect the transcriptional response to changes in diet quantity, and so should be considered in future studies that explore the effect of nutrition on body size.

     
    more » « less
  3. Abstract Background The red sea urchin Mesocentrotus franciscanus is an ecologically important kelp forest herbivore and an economically valuable wild fishery species. To examine how M. franciscanus responds to its environment on a molecular level, differences in gene expression patterns were observed in embryos raised under combinations of two temperatures (13 °C or 17 °C) and two p CO 2 levels (475 μatm or 1050 μatm). These combinations mimic various present-day conditions measured during and between upwelling events in the highly dynamic California Current System with the exception of the 17 °C and 1050 μatm combination, which does not currently occur. However, as ocean warming and acidification continues, warmer temperatures and higher p CO 2 conditions are expected to increase in frequency and to occur simultaneously. The transcriptomic responses of the embryos were assessed at two developmental stages (gastrula and prism) in light of previously described plasticity in body size and thermotolerance under these temperature and p CO 2 treatments. Results Although transcriptomic patterns primarily varied by developmental stage, there were pronounced differences in gene expression as a result of the treatment conditions. Temperature and p CO 2 treatments led to the differential expression of genes related to the cellular stress response, transmembrane transport, metabolic processes, and the regulation of gene expression. At each developmental stage, temperature contributed significantly to the observed variance in gene expression, which was also correlated to the phenotypic attributes of the embryos. On the other hand, the transcriptomic response to p CO 2 was relatively muted, particularly at the prism stage. Conclusions M. franciscanus exhibited transcriptomic plasticity under different temperatures, indicating their capacity for a molecular-level response that may facilitate red sea urchins facing ocean warming as climate change continues. In contrast, the lack of a robust transcriptomic response, in combination with observations of decreased body size, under elevated p CO 2 levels suggest that this species may be negatively affected by ocean acidification. High present-day p CO 2 conditions that occur due to coastal upwelling may already be influencing populations of M. franciscanus . 
    more » « less
  4. Abstract Different intensities of high temperatures affect the growth of photosynthetic cells in nature. To elucidate the underlying mechanisms, we cultivated the unicellular green alga Chlamydomonas reinhardtii under highly controlled photobioreactor conditions and revealed systems-wide shared and unique responses to 24-hour moderate (35°C) and acute (40°C) high temperatures and subsequent recovery at 25°C. We identified previously overlooked unique elements in response to moderate high temperature. Heat at 35°C transiently arrested the cell cycle followed by partial synchronization, up-regulated transcripts/proteins involved in gluconeogenesis/glyoxylate-cycle for carbon uptake and promoted growth. But 40°C disrupted cell division and growth. Both high temperatures induced photoprotection, while 40°C distorted thylakoid/pyrenoid ultrastructure, affected the carbon concentrating mechanism, and decreased photosynthetic efficiency. We demonstrated increased transcript/protein correlation during both heat treatments and hypothesize reduced post-transcriptional regulation during heat may help efficiently coordinate thermotolerance mechanisms. During recovery after both heat treatments, especially 40°C, transcripts/proteins related to DNA synthesis increased while those involved in photosynthetic light reactions decreased. We propose down-regulating photosynthetic light reactions during DNA replication benefits cell cycle resumption by reducing ROS production. Our results provide potential targets to increase thermotolerance in algae and crops. 
    more » « less
  5. Abstract

    The molecular machinery for protein synthesis is profoundly similar between plants and other eukaryotes. Mechanisms of translational gene regulation are embedded into the broader network of RNA‐level processes including RNA quality control and RNA turnover. However, over eons of their separate history, plants acquired new components, dropped others, and generally evolved an alternate way of making the parts list of protein synthesis work. Research over the past 5 years has unveiled how plants utilize translational control to defend themselves against viruses, regulate translation in response to metabolites, and reversibly adjust translation to a wide variety of environmental parameters. Moreover, during seed and pollen development plants make use of RNA granules and other translational controls to underpin developmental transitions between quiescent and metabolically active stages. The economics of resource allocation over the daily light–dark cycle also include controls over cellular protein synthesis. Important new insights into translational control on cytosolic ribosomes continue to emerge from studies of translational control mechanisms in viruses. Finally, sketches of coherent signaling pathways that connect external stimuli with a translational response are emerging, anchored in part around TOR and GCN2 kinase signaling networks. These again reveal some mechanisms that are familiar and others that are different from other eukaryotes, motivating deeper studies on translational control in plants.

    This article is categorized under:

    Translation > Translation Regulation

    RNA Structure and Dynamics > Influence of RNA Structure in Biological Systems

    RNA Interactions with Proteins and Other Molecules > Protein‐RNA Interactions: Functional Implications

     
    more » « less