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Publikation

Winkler, M., Niemeyer, M., Hellmuth, A., Janitza, P., Christ, G., Samodelov, S. L., Wilde, V., Majovsky, P., Trujillo, M., Zurbriggen, M. D., Hoehenwarter, W., Quint, M. & Calderón Villalobos, L. I. A. Variation in auxin sensing guides AUX/IAA transcriptional repressor ubiquitylation and destruction. Nature Commun. 8, 15706, (2017) DOI: 10.1038/ncomms15706

Auxin is a small molecule morphogen that bridges SCFTIR1/AFB-AUX/IAA co-receptor interactions leading to ubiquitylation and proteasome-dependent degradation of AUX/IAA transcriptional repressors. Here, we systematically dissect auxin sensing by SCFTIR1-IAA6 and SCFTIR1-IAA19 co-receptor complexes, and assess IAA6/IAA19 ubiquitylation in vitro and IAA6/IAA19 degradation in vivo. We show that TIR1-IAA19 and TIR1-IAA6 have distinct auxin affinities that correlate with ubiquitylation and turnover dynamics of the AUX/IAA. We establish a system to track AUX/IAA ubiquitylation in IAA6 and IAA19 in vitro and show that it occurs in flexible hotspots in degron-flanking regions adorned with specific Lys residues. We propose that this signature is exploited during auxin-mediated SCFTIR1-AUX/IAA interactions. We present evidence for an evolving AUX/IAA repertoire, typified by the IAA6/IAA19 ohnologues, that discriminates the range of auxin concentrations found in plants. We postulate that the intrinsic flexibility of AUX/IAAs might bias their ubiquitylation and destruction kinetics enabling specific auxin responses.
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

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

Drost, H.-G., Bellstädt, J., Ó'Maoiléidigh, D. S., Silva, A. T., Gabel, A., Weinholdt, C., Ryan, P. T., Dekkers, B. J. W., Bentsink, L., Hilhorst, H. W. M., Ligterink, W., Wellmer, F., Grosse, I. & Quint, M. Post-embryonic Hourglass Patterns Mark Ontogenetic Transitions in Plant Development Mol Biol Evol 33, 1158-1163, (2016) DOI: 10.1093/molbev/msw039

The historic developmental hourglass concept depicts the convergence of animal embryos to a common form during the phylotypic period. Recently, it has been shown that a transcriptomic hourglass is associated with this morphological pattern, consistent with the idea of underlying selective constraints due to intense molecular interactions during body plan establishment. Although plants do not exhibit a morphological hourglass during embryogenesis, a transcriptomic hourglass has nevertheless been identified in the model plant Arabidopsis thaliana. Here, we investigated whether plant hourglass patterns are also found postembryonically. We found that the two main phase changes during the life cycle of Arabidopsis, from embryonic to vegetative and from vegetative to reproductive development, are associated with transcriptomic hourglass patterns. In contrast, flower development, a process dominated by organ formation, is not. This suggests that plant hourglass patterns are decoupled from organogenesis and body plan establishment. Instead, they may reflect general transitions through organizational checkpoints. 

Publikation

Kowalski, A. M., Gooding, M., Ferrante, A., Slafer, G. A., Orford, S., Gasperini, D. & Griffiths, S. Agronomic assessment of the wheat semi-dwarfing gene Rht8 in contrasting nitrogen treatments and water regimes Field Crop Res 191, 150-160, (2016) DOI: 10.1016/j.fcr.2016.02.026

Reduced height 8 (Rht8) is the main alternative to the GA-insensitive Rht alleles in hot and dry environments where it reduces plant height without yield penalty. The potential of Rht8 in northern-European wheat breeding remains unclear, since the close linkage with the photoperiod-insensitive allele Ppd-D1a is unfavourable in the relatively cool summers. In the present study, two near-isogenic lines (NILs) contrasting for the Rht8/tall allele from Mara in a UK-adapted and photoperiod-sensitive wheat variety were evaluated in trials with varying nitrogen fertiliser (N) treatments and water regimes across sites in the UK and Spain.

The Rht8 introgression was associated with a robust height reduction of 11% regardless of N treatment and water regime and the Rht8 NIL was more resistant to root-lodging at agronomically-relevant N levels than the tall NIL. In the UK with reduced solar radiation over the growing season than the site in Spain, the Rht8 NIL showed a 10% yield penalty at standard agronomic N levels due to concomitant reduction in grain number and spike number whereas grain weight and harvest index were not significantly different to the tall NIL. The yield penalty associated with the Rht8 introgression was overcome at low N and in irrigated conditions in the UK, and in the high-temperature site in Spain. Decreased spike length and constant spikelet number in the Rht8 NIL resulted in spike compaction of 15%, independent of N and water regime. The genetic interval of Rht8 overlaps with the compactum gene on 2DS, raising the possibility of the same causative gene. Further genetic dissection of these loci is required.

Abbreviations

    ANOVA, analysis of variance; Y, yield; HI, harvest index; GN, grain number (m−2); SS, spikelet number (spike−1); SN, spike number (m−2); HD, heading date; AN, anthesis; 12L, length of the second internode from the top; 13L, length of the third internode from the top; PAR, photosynthetically active radiation; R: FR, red: far-red light reflectance ratio; RCBD, randomised complete block design

Publikation

Gasperini, D. & Acosta, I. F. and Farmer, E. E. Cotyledon Wounding of Arabidopsis Seedlings. Bio-protocol 6 (2), e1712, (2016)


Publikation

Drost, H.-G., Gabel, A., Grosse, I. & Quint, M. Evidence for Active Maintenance of Phylotranscriptomic Hourglass Patterns in Animal and Plant Embryogenesis Mol Biol Evol 32, 1221-1231, (2015) DOI: 10.1093/molbev/msv012

The developmental hourglass model has been used to describe the morphological transitions of related species throughout embryogenesis. Recently, quantifiable approaches combining transcriptomic and evolutionary information provided novel evidence for the presence of a phylotranscriptomic hourglass pattern across kingdoms. As its biological function is unknown it remains speculative whether this pattern is functional or merely represents a nonfunctional evolutionary relic. The latter would seriously hamper future experimental approaches designed to test hypotheses regarding its function. Here, we address this question by generating transcriptome divergence index (TDI) profiles across embryogenesis of Danio rerio, Drosophila melanogaster, and Arabidopsis thaliana. To enable meaningful evaluation of the resulting patterns, we develop a statistical test that specifically assesses potential hourglass patterns. Based on this objective measure we find that two of these profiles follow a statistically significant hourglass pattern with the most conserved transcriptomes in the phylotypic periods. As the TDI considers only recent evolutionary signals, this indicates that the phylotranscriptomic hourglass pattern is not a rudiment but possibly actively maintained, implicating the existence of some linked biological function associated with embryogenesis in extant species.

Publikation

Gasperini, D., Chauvin, A., Acosta, I.F., Kurenda, A., Stolz, S., Chétalat, A., Wolfender J.-L. & Farmer, E.E. Axial and Radial Oxylipin Transport. Plant Physiol. 169, 2244-2254, (2015) DOI: 10.1104/pp.15.01104

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Publikation

Gasperini, D., Chételat, A., Acosta, I.F., Goossens, J., Pauwels, L., Goossens, A., Dreos, R., Alonso, E. & Farmer, E.E. Multilayered Organization of Jasmonate Signalling in the Regulation of Root Growth PLoS Genet. 11 (6), e1005300, (2015) DOI: 10.1371/journal.pgen.1005300

Physical damage can strongly affect plant growth, reducing the biomass of developing organs situated at a distance from wounds. These effects, previously studied in leaves, require the activation of jasmonate (JA) signalling. Using a novel assay involving repetitive cotyledon wounding in Arabidopsis seedlings, we uncovered a function of JA in suppressing cell division and elongation in roots. Regulatory JA signalling components were then manipulated to delineate their relative impacts on root growth. The new transcription factor mutant myc2-322B was isolated. In vitro transcription assays and whole-plant approaches revealed that myc2-322B is a dosage-dependent gain-of-function mutant that can amplify JA growth responses. Moreover, myc2-322B displayed extreme hypersensitivity to JA that totally suppressed root elongation. The mutation weakly reduced root growth in undamaged plants but, when the upstream negative regulator NINJA was genetically removed, myc2-322B powerfully repressed root growth through its effects on cell division and cell elongation. Furthermore, in a JA-deficient mutant background, ninja1 myc2-322B still repressed root elongation, indicating that it is possible to generate JA-responses in the absence of JA. We show that NINJA forms a broadly expressed regulatory layer that is required to inhibit JA signalling in the apex of roots grown under basal conditions. By contrast, MYC2, MYC3 and MYC4 displayed cell layer-specific localisations and MYC3 and MYC4 were expressed in mutually exclusive regions. In nature, growing roots are likely subjected to constant mechanical stress during soil penetration that could lead to JA production and subsequent detrimental effects on growth. Our data reveal how distinct negative regulatory layers, including both NINJA-dependent and -independent mechanisms, restrain JA responses to allow normal root growth. Mechanistic insights from this work underline the importance of mapping JA signalling components to specific cell types in order to understand and potentially engineer the growth reduction that follows physical damage.

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. 

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