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Publikation

Quint, M., Delker, C., Franklin, K. A., Wigge, P. A., Halliday, K. J. & van Zanten, M. Molecular and genetic control of plant thermomorphogenesis. Nat Plants 2, 15190, (2016) DOI: 10.1038/nplants.2015.190

Temperature is a major factor governing the distribution and seasonal behaviour of plants. Being sessile, plants are highly responsive to small differences in temperature and adjust their growth and development accordingly. The suite of morphological and architectural changes induced by high ambient temperatures, below the heat-stress range, is collectively called thermomorphogenesis. Understanding the molecular genetic circuitries underlying thermomorphogenesis is particularly relevant in the context of climate change, as this knowledge will be key to rational breeding for thermo-tolerant crop varieties. Until recently, the fundamental mechanisms of temperature perception and signalling remained unknown. Our understanding of temperature signalling is now progressing, mainly by exploiting the model plant Arabidopsis thaliana. The transcription factor PHYTOCHROME INTERACTING FACTOR 4 (PIF4) has emerged as a critical player in regulating phytohormone levels and their activity. To control thermomorphogenesis, multiple regulatory circuits are in place to modulate PIF4 levels, activity and downstream mechanisms. Thermomorphogenesis is integrally governed by various light signalling pathways, the circadian clock, epigenetic mechanisms and chromatin-level regulation. In this Review, we summarize recent progress in the field and discuss how the emerging knowledge in Arabidopsis may be transferred to relevant crop systems.

The year 2015 is on track to surpass 2014 as the warmest year ever recorded since systematic temperature measurements began more than a century ago1. In fact, the 10 warmest years on record all occurred after 1998. The fifth report of the Intergovernmental Panel on Climate Change2 projects an increase of 0.8–4.8 °C in global mean surface temperature within the twenty-first century. Such figures are alarming as it is expected that this will strongly affect plant distribution and survival, and therefore threaten biodiversity3,​4,​5,​6,​7,​8,​9,​10,​11. Some studies already indicate that plant species unable to adjust flowering time in response to temperature are disappearing from certain environments5, and species tend to shift to higher altitudes and latitudes12.

Likewise, crop productivity will probably suffer greatly from global warming, while food production is required to increase significantly to sustain a growing and more demanding world population9,13,​14,​15. A meta-analysis summarizing more than 1,700 studies on the effects of climate change and adaptations on crop yields revealed consensus that in the second half of this century, climate warming is likely to have a negative effect on yields of important staple crops13.

Breeding for crop-level adaptations to cope with high temperatures could potentially reverse this negative trend9,13,​14,​15. In several plant species, mechanisms have evolved to adapt growth and morphology to stimulate mitigation of warmth through enhanced evaporative cooling, increased convection and direct avoidance of heat flux from the Sun16,​17,​18,​19,​20. If understood, the underlying molecular processes of these so-called thermomorphogenesis responses could be attractive breeding targets for improving crops to withstand climate warming.

Although abundant literature is available on how plants tolerate extreme heat stress (reviewed in refs 9,21), we are only beginning to understand the molecular mechanisms underlying thermomorphogenesis in response to moderately increased temperatures. A key breakthrough was the identification of the bHLH (basic helix–loop–helix) transcription factor PHYTOCHROME INTERACTING FACTOR 4 (PIF4) as a central regulator of ambient temperature signalling in Arabidopsis22. Recent findings have implicated important roles for light signalling pathways, the circadian clock23,​24,​25,​26,​27,​28, auxin22,29,​30,​31 and other phytohormones31,​32,​33,​34 in PIF4-mediated temperature-induced growth. Furthermore, epigenetic mechanisms appear at the nexus of induction35 and attenuation36 of growth acclimation in response to high ambient temperatures.

Here we discuss and integrate recent findings on the molecular networks driving thermomorphogenic adaptations. We will highlight missing links and suggest how the knowledge on Arabidopsis could be transferred to crops. In addition to thermomorphogenesis, adaptation to high ambient temperature also involves physiological processes such as photosynthetic acclimation, respiration and changes in carbon balance. For discussions of these topics as well as on phenological changes including premature flowering, we refer the reader to reviews elsewhere20,37,​38,​39.

Publikation

Trenner, J., Poeschl, Y., Grau, J., Gogol-Döring, A., Quint, M. & Delker, C. Auxin-induced expression divergence between Arabidopsis species may originate within the TIR1/AFB–AUX/IAA–ARF module J. Exp. Bot. 68, 539-552, (2016) DOI: 10.1093/jxb/erw457

Auxin is an essential regulator of plant growth and development, and auxin signaling components are conserved among land plants. Yet, a remarkable degree of natural variation in physiological and transcriptional auxin responses has been described among Arabidopsis thaliana accessions. As intraspecies comparisons offer only limited genetic variation, we here inspect the variation of auxin responses between A. thaliana and A. lyrata. This approach allowed the identification of conserved auxin response genes including novel genes with potential relevance for auxin biology. Furthermore, promoter divergences were analyzed for putative sources of variation. De novo motif discovery identified novel and variants of known elements with potential relevance for auxin responses, emphasizing the complex, and yet elusive, code of element combinations accounting for the diversity in transcriptional auxin responses. Furthermore, network analysis revealed correlations of interspecies differences in the expression of AUX/IAA gene clusters and classic auxin-related genes. We conclude that variation in general transcriptional and physiological auxin responses may originate substantially from functional or transcriptional variations in the TIR1/AFB, AUX/IAA, and ARF signaling network. In that respect, AUX/IAA gene expression divergence potentially reflects differences in the manner in which different species transduce identical auxin signals into gene expression responses.

Publikation

Raschke, A., Ibañez, C., Ullrich, K., Anwer, M., Becker, S., Glöckner, A., Trenner, J., Denk, K., Saal, B., Sun, X., Ni, M., Davis, S., Delker, C. & Quint, M. Natural variants of ELF3 affect thermomorphogenesis by transcriptionally modulating PIF4-dependent auxin response genes BMC Plant Biol. 15, 197, (2015) DOI: 10.1186/s12870-015-0566-6

Background

Perception and transduction of temperature changes result in altered growth enabling plants to adapt to increased ambient temperature. While PHYTOCHROME-INTERACTING FACTOR4 (PIF4) has been identified as a major ambient temperature signaling hub, its upstream regulation seems complex and is poorly understood. Here, we exploited natural variation for thermo-responsive growth in Arabidopsis thaliana using quantitative trait locus (QTL) analysis.

Results

We identified GIRAFFE2.1, a major QTL explaining ~18 % of the phenotypic variation for temperature-induced hypocotyl elongation in the Bay-0 x Sha recombinant inbred line population. Transgenic complementation demonstrated that allelic variation in the circadian clock regulator EARLY FLOWERING3 (ELF3) is underlying this QTL. The source of variation could be allocated to a single nucleotide polymorphism in the ELF3 coding region, resulting in differential expression of PIF4 and its target genes, likely causing the observed natural variation in thermo-responsive growth.

ConclusionsIn combination with other recent studies, this work establishes the role of ELF3 in the ambient temperature signaling network. Natural variation of ELF3-mediated gating of PIF4 expression during nightly growing periods seems to be affected by a coding sequence quantitative trait nucleotide that confers a selective advantage in certain environments. In addition, natural ELF3 alleles seem to differentially integrate temperature and photoperiod information to induce architectural changes. Thus, ELF3 emerges as an essential coordinator of growth and development in response to diverse environmental cues and implicates ELF3 as an important target of adaptation. 

Publikation

Delker, C., Sonntag, L., Geo, V. J., Janitza, P., Ibañez, C., Ziermann, H., Peterson, T., Denk, K., Mull, S., Ziegler, J., Davis, S. J., Schneeberger, K. & Quint, M. The DET1-COP1-HY5 Pathway Constitutes a Multipurpose Signaling Module Regulating Plant Photomorphogenesis and Thermomorphogenesis Cell Rep 9, 1983–1989, (2014) DOI: 10.1016/j.celrep.2014.11.043

Developmental plasticity enables plants to respond to elevated ambient temperatures by adapting their shoot architecture. On the cellular level, the basic-helix-loop-helix (bHLH) transcription factor PHYTOCHROME INTERACTING FACTOR 4 (PIF4) coordinates this response by activating hormonal modules that in turn regulate growth. In addition to an unknown temperature-sensing mechanism, it is currently not understood how temperature regulates PIF4 activity. Using a forward genetic approach in Arabidopsis thaliana, we present extensive genetic evidence demonstrating that the DE-ETIOLATED 1 (DET1)-CONSTITUTIVE PHOTOMORPHOGENIC 1 (COP1)-ELONGATED HYPOCOTYL 5 (HY5)-dependent photomorphogenesis pathway transcriptionally regulates PIF4 to coordinate seedling growth in response to elevated temperature. Our findings demonstrate that two of the most prevalent environmental cues, light and temperature, share a much larger set of signaling components than previously assumed. Similar to the toolbox concept in animal embryonic patterning, multipurpose signaling modules might have evolved in plants to translate various environmental stimuli into adaptational growth processes

Publikation

Poeschl, Y., Delker, C., Trenner, J., Ullrich, K. & Quint, M. & Grosse, I. Optimized probe masking for comparative transcriptomics of closely related species. PLOS ONE 8, e78497, (2013)

Microarrays are commonly applied to study the transcriptome of specific species. However, many available microarrays are

restricted to model organisms, and the design of custom microarrays for other species is often not feasible. Hence,

transcriptomics approaches of non-model organisms as well as comparative transcriptomics studies among two or more

species often make use of cost-intensive RNAseq studies or, alternatively, by hybridizing transcripts of a query species to a

microarray of a closely related species. When analyzing these cross-species microarray expression data, differences in the

transcriptome of the query species can cause problems, such as the following: (i) lower hybridization accuracy of probes due

to mismatches or deletions, (ii) probes binding multiple transcripts of different genes, and (iii) probes binding transcripts of

non-orthologous genes. So far, methods for (i) exist, but these neglect (ii) and (iii). Here, we propose an approach for

comparative transcriptomics addressing problems (i) to (iii), which retains only transcript-specific probes binding transcripts

of orthologous genes. We apply this approach to an Arabidopsis lyrata expression data set measured on a microarray

designed for Arabidopsis thaliana, and compare it to two alternative approaches, a sequence-based approach and a genomic

DNA hybridization-based approach. We investigate the number of retained probe sets, and we validate the resulting

expression responses by qRT-PCR. We find that the proposed approach combines the benefit of sequence-based stringency

and accuracy while allowing the expression analysis of much more genes than the alternative sequence-based approach. As

an added benefit, the proposed approach requires probes to detect transcripts of orthologous genes only, which provides asuperior base for biological interpretation of the measured expression responses.

Publikation

Delker, C. & Quint, M. Expression level polymorphisms: heritable traits shaping natural variation Trends Plant Sci 16, 481-488, (2011)

Natural accessions of many species harbor a wealth of genetic variation visible in a large array of phenotypes. Although expression level polymorphisms (ELPs) in several genes have been shown to contribute to variation in diverse traits, their general impact on adaptive variation has likely been underestimated. At present, ELPs have predominantly been correlated to quantitative trait loci (eQTLs) that occupy central hubs in signaling networks, which pleiotropically affect numerous traits. To increase the sensitivity of detecting minor effect eQTLs or those that act in a trait-specific manner, we emphasize the need for more systematic approaches. This requires, but is not limited to, refining experimental designs such as reduction of tissue complexity and combinatorial methods including a priori defined networks.

Publikation

Delker, C., Pöschl, Y., Raschke, A., Ullrich, K., Ettingshausen, S., Hauptmann, V., Grosse, I. & Quint, M. Natural variation of transcriptional auxin response networks in Arabidopsis thaliana Plant Cell 22, 2184-2200, (2010)

Natural variation has been observed for various traits in Arabidopsis thaliana. Here, we investigated natural variation in the context of physiological and transcriptional responses to the phytohormone auxin, a key regulator of plant development. A survey of the general extent of natural variation to auxin stimuli revealed significant physiological variation among 20 genetically diverse natural accessions. Moreover, we observed dramatic variation on the global transcriptome level after induction of auxin responses in seven accessions. Although we detect isolated cases of major-effect polymorphisms, sequencing of signaling genes revealed sequence conservation, making selective pressures that favor functionally different protein variants among accessions unlikely. However, coexpression analyses of a priori defined auxin signaling networks identified variations in the transcriptional equilibrium of signaling components. In agreement with this, cluster analyses of genome-wide expression profiles followed by analyses of a posteriori defined gene networks revealed accession-specific auxin responses. We hypothesize that quantitative distortions in the ratios of interacting signaling components contribute to the detected transcriptional variation, resulting in physiological variation of auxin responses among accessions.

Publikation

Leon-Reyes, A., Van der Does, D., De Lange, E.S., Delker, C., Wasternack, C., Van Wees, S.C., Ritsema, T. & Pieterse, C.M. Salicylate-mediated suppression of jasmonate-responsive gene expression in Arabidopsis is targeted downstream of the jasmonate biosynthesis pathway Planta 232(6), 1423-1432, (2010)

Jasmonates (JAs) and salicylic acid (SA) are plant hormones that play pivotal roles in the regulation of induced defenses against microbial pathogens and insect herbivores. Their signaling pathways cross-communicate providing the plant with a regulatory potential to finely tune its defense response to the attacker(s) encountered. In Arabidopsis thaliana, SA strongly antagonizes the jasmonic acid (JA) signaling pathway, resulting in the downregulation of a large set of JA-responsive genes, including the marker genes PDF1.2 and VSP2. Induction of JA-responsive marker gene expression by different JA derivatives was equally sensitive to SA-mediated suppression. Activation of genes encoding key enzymes in the JA biosynthesis pathway, such as LOX2, AOS, AOC2, and OPR3 was also repressed by SA, suggesting that the JA biosynthesis pathway may be a target for SA-mediated antagonism. To test this, we made use of the mutant aos/dde2, which is completely blocked in its ability to produce JAs because of a mutation in the ALLENE OXIDE SYNTHASE gene. Mutant aos/dde2 plants did not express the JA-responsive marker genes PDF1.2 or VSP2 in response to infection with the necrotrophic fungus Alternaria brassicicola or the herbivorous insect Pieris rapae. Bypassing JA biosynthesis by exogenous application of methyl jasmonate (MeJA) rescued this JA-responsive phenotype in aos/dde2. Application of SA suppressed MeJA-induced PDF1.2 expression to the same level in the aos/dde2 mutant as in wild-type Col-0 plants, indicating that SA-mediated suppression of JAresponsive gene expression is targeted at a position downstream of the JA biosynthesis pathway.

Publikation

Delker, C., Raschke, A. & Quint, M. Auxin dynamics: the dazzling complexity of a small molecule's message Planta 227, 929-941 , (2008)

The phytohormone auxin is a potent regulator of plant development. Since its discovery in the beginning of the twentieth century many aspects of auxin biology have been extensively studied, ranging from biosynthesis and metabolism to the elucidation of molecular components of downstream signaling. With the identification of the F-box protein TIR1 as an auxin receptor a major breakthrough in understanding auxin signaling has been achieved and recent modeling approaches have shed light on the putative mechanisms underlying the establishment of auxin gradients and maxima essential for many auxin-regulated processes. Here, we review these and other recent advances in unraveling the entanglement of biosynthesis, polar transport and cellular signaling events that allow small auxinic molecules to facilitate their complex regulatory action.

Publikation

Delker, C., Zolman, B.K., Miersch, O. & Wasternack, C. Jasmonate biosynthesis in Arabidopsis thaliana requires peroxisomal beta-oxidation enzymes Additional proof by properties of pex6 and aim1 Phytochemistry 68, 1642-1650, (2007)

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