Artículo

Pucciariello, O.; Legris, M.; Rojas, C.C.; Iglesias, M.J.; Hernando, C.E.; Dezar, C.; Vazquez, M.; Yanovsky, M.J.; Finlayson, S.A.; Prat, S.; Casal, J.J. "Rewiring of auxin signaling under persistent shade" (2018) Proceedings of the National Academy of Sciences of the United States of America. 115(21):5612-5617
El editor solo permite decargar el artículo en su versión post-print desde el repositorio. Por favor, si usted posee dicha versión, enviela a
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

Light cues from neighboring vegetation rapidly initiate plant shade-avoidance responses. Despite our detailed knowledge of the early steps of this response, the molecular events under prolonged shade are largely unclear. Here we show that persistent neighbor cues reinforce growth responses in addition to promoting auxin-responsive gene expression in Arabidopsis and soybean. However, while the elevation of auxin levels is well established as an early event, in Arabidopsis, the response to prolonged shade occurs when auxin levels have declined to the pres-timulation values. Remarkably, the sustained low activity of phytochrome B under prolonged shade led to (i) decreased levels of PHYTOCHROME INTERACTING FACTOR 4 (PIF4) in the cotyledons (the organs that supply auxin) along with increased levels in the vascular tissues of the stem, (ii) elevated expression of the PIF4 targets INDOLE-3-ACETIC ACID 19 (IAA19) and IAA29, which in turn reduced the expression of the growth-repressive IAA17 regulator, (iii) reduced abundance of AUXIN RESPONSE FACTOR 6, (iv) reduced expression of MIR393 and increased abundance of its targets, the auxin receptors, and (v) elevated auxin signaling as indicated by molecular markers. Mathematical and genetic analyses support the physiological role of this system-level rearrangement. We propose that prolonged shade rewires the connectivity between light and auxin signaling to sustain shade avoidance without enhanced auxin levels. © 2018 National Academy of Sciences. All Rights Reserved.

Registro:

Documento: Artículo
Título:Rewiring of auxin signaling under persistent shade
Autor:Pucciariello, O.; Legris, M.; Rojas, C.C.; Iglesias, M.J.; Hernando, C.E.; Dezar, C.; Vazquez, M.; Yanovsky, M.J.; Finlayson, S.A.; Prat, S.; Casal, J.J.
Filiación:Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura (IFEVA), Facultad de Agronomía, Universidad de Buenos Aires, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina
Fundación Instituto Leloir, Instituto de Investigaciones Bioquímicas de Buenos Aires, CONICET, Buenos Aires, Argentina
Instituto de Agrobiotecnología de Rosario, CONICET, Rosario, Argentina
Department of Soil and Crop Sciences, Texas A and M University, College Station, TX, United States
Faculty of Molecular and Environmental Plant Sciences, Texas A and M University, College Station, TX, United States
Departamento de Genética Molecular de Plantas, Centro Nacional de Biotecnología, Consejo Superior de Investigaciones Científicas, Madrid, Spain
Center for Integrative Genomics, Faculty of Biology and Medicine, University of Lausanne, Lausanne, Switzerland
Instituto de Investigaciones Biológicas, Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata and CONICET, Mar del Plata, Argentina
Palabras clave:Aux/IAA; Auxin receptor; MIR393; Phytochrome B; PIF4
Año:2018
Volumen:115
Número:21
Página de inicio:5612
Página de fin:5617
DOI: http://dx.doi.org/10.1073/pnas.1721110115
Título revista:Proceedings of the National Academy of Sciences of the United States of America
Título revista abreviado:Proc. Natl. Acad. Sci. U. S. A.
ISSN:00278424
CODEN:PNASA
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00278424_v115_n21_p5612_Pucciariello

Referencias:

  • Fraser, D.P., Hayes, S., Franklin, K.A., Photoreceptor crosstalk in shade avoidance (2016) Curr Opin Plant Biol, 33, pp. 1-7
  • Casal, J.J., Photoreceptor signaling networks in plant responses to shade (2013) Annu Rev Plant Biol, 64, pp. 403-427
  • Ballaré, C.L., Pierik, R., The shade-avoidance syndrome: Multiple signals and ecological consequences (2017) Plant Cell Environ, 40, pp. 2530-2543
  • López Pereira, M., Sadras, V.O., Batista, W., Casal, J.J., Hall, A.J., Light-mediated self-organization of sunflower stands increases oil yield in the field (2017) Proc Natl Acad Sci USA, 114, pp. 7975-7980
  • Leivar, P., Quail, P.H., PIFs: Pivotal components in a cellular signaling hub (2011) Trends Plant Sci, 16, pp. 19-28
  • Lee, N., Choi, G., Phytochrome-interacting factor from Arabidopsis to liverwort (2017) Curr Opin Plant Biol, 35, pp. 54-60
  • Leivar, P., Monte, E., Cohn, M.M., Quail, P.H., Phytochrome signaling in green Arabidopsis seedlings: Impact assessment of a mutually negative phyB-PIF feedback loop (2012) Mol Plant, 5, pp. 734-749
  • Lorrain, S., Allen, T., Duek, P.D., Whitelam, G.C., Fankhauser, C., Phytochrome-mediated inhibition of shade avoidance involves degradation of growth-promoting bHLH transcription factors (2008) Plant J, 53, pp. 312-323
  • Li, L., Linking photoreceptor excitation to changes in plant architecture (2012) Genes Dev, 26, pp. 785-790
  • Pedmale, U.V., Cryptochromes interact directly with PIFs to control plant growth in limiting blue light (2016) Cell, 164, pp. 233-245
  • De Wit, M., Integration of phytochrome and cryptochrome signals determines plant growth during competition for light (2016) Curr Biol, 26, pp. 3320-3326
  • Hornitschek, P., Phytochrome interacting factors 4 and 5 control seedling growth in changing light conditions by directly controlling auxin signaling (2012) Plant J, 71, pp. 699-711
  • Zhang, Y., A quartet of PIF bHLH factors provides a transcriptionally centered signaling hub that regulates seedling morphogenesis through differential expression-patterning of shared target genes in Arabidopsis (2013) PLoS Genet, 9
  • Tao, Y., Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants (2008) Cell, 133, pp. 164-176
  • Procko, C., Crenshaw, C.M., Ljung, K., Noel, J.P., Chory, J., Cotyledon-generated auxin is required for shade-induced hypocotyl growth in Brassica rapa (2014) Plant Physiol, 165, pp. 1285-1301
  • Keuskamp, D.H., Pollmann, S., Voesenek, L.A.C.J., Peeters, A.J.M., Pierik, R., Auxin transport through PIN-FORMED 3 (PIN3) controls shade avoidance and fitness during competition (2010) Proc Natl Acad Sci USA, 107, pp. 22740-22744
  • Procko, C., The epidermis coordinates auxin-induced stem growth in response to shade (2016) Genes Dev, 30, pp. 1529-1541
  • Michaud, O., Fiorucci, A.S., Xenarios, I., Fankhauser, C., Local auxin production underlies a spatially restricted neighbor-detection response in Arabidopsis (2017) Proc Natl Acad Sci USA, 114, pp. 7444-7449
  • Pantazopoulou, C.K., Neighbor detection at the leaf tip adaptively regulates upward leaf movement through spatial auxin dynamics (2017) Proc Natl Acad Sci USA, 114, pp. 7450-7455
  • Lavy, M., Estelle, M., Mechanisms of auxin signaling (2016) Development, 143, pp. 3226-3229
  • Weijers, D., Wagner, D., Transcriptional responses to the auxin hormone (2016) Annu Rev Plant Biol, 67, pp. 539-574
  • Middleton, A.M., King, J.R., Bennett, M.J., Owen, M.R., Mathematical modelling of the Aux/IAA negative feedback loop (2010) Bull Math Biol, 72, pp. 1383-1407
  • Vernoux, T., The auxin signalling network translates dynamic input into robust patterning at the shoot apex (2011) Mol Syst Biol, 7, p. 508
  • Winkler, M., Variation in auxin sensing guides AUX/IAA transcriptional repressor ubiquitylation and destruction (2017) Nat Commun, 8, p. 15706
  • Navarro, L., A plant miRNA contributes to antibacterial resistance by repressing auxin signaling (2006) Science, 312, pp. 436-439
  • Si-Ammour, A., MiR393 and secondary siRNAs regulate expression of the TIR1/AFB2 auxin receptor clade and auxin-related development of Arabidopsis leaves (2011) Plant Physiol, 157, pp. 683-691
  • Morgan, D.C., Smith, H., The relationship between phytochrome-photoequilibrium and development in light grown Chenopodium album L (1978) Planta, 142, pp. 187-193
  • Das, D., St Onge, K.R., Voesenek, L.A., Pierik, R., Sasidharan, R., Ethylene- And shade-induced hypocotyl elongation share transcriptome patterns and functional regulators (2016) Plant Physiol, 172, pp. 718-733
  • Bou-Torrent, J., Plant proximity perception dynamically modulates hormone levels and sensitivity in Arabidopsis (2014) J Exp Bot, 65, pp. 2937-2947
  • De Wit, M., Ljung, K., Fankhauser, C., Contrasting growth responses in lamina and petiole during neighbor detection depend on differential auxin responsiveness rather than different auxin levels (2015) New Phytol, 208, pp. 198-209
  • Klose, C., Systematic analysis of how phytochrome B dimerization determines its specificity (2015) Nat Plants, 1, p. 15090
  • Hornitschek, P., Lorrain, S., Zoete, V., Michielin, O., Fankhauser, C., Inhibition of the shade avoidance response by formation of non-DNA binding bHLH heterodimers (2009) EMBO J, 28, pp. 3893-3902
  • Nusinow, D.A., The ELF4-ELF3-LUX complex links the circadian clock to diurnal control of hypocotyl growth (2011) Nature, 475, pp. 398-402
  • Nieto, C., López-Salmerón, V., Davière, J.-M., Prat, S., ELF3-PIF4 interaction regulates plant growth independently of the evening complex (2015) Curr Biol, 25, pp. 187-193
  • Pacín, M., Semmoloni, M., Legris, M., Finlayson, S.A., Casal, J.J., Convergence of CONSTITUTIVE PHOTOMORPHOGENESIS 1 and PHYTOCHROME INTERACTING FACTOR signalling during shade avoidance (2016) New Phytol, 211, pp. 967-979
  • Tatematsu, K., MASSUGU2 encodes Aux/IAA19, an auxin-regulated protein that functions together with the transcriptional activator NPH4/ARF7 to regulate differential growth responses of hypocotyl and formation of lateral roots in Arabidopsis thaliana (2004) Plant Cell, 16, pp. 379-393
  • Krogan, N.T., Yin, X., Ckurshumova, W., Berleth, T., Distinct subclades of Aux/IAA genes are direct targets of ARF5/MP transcriptional regulation (2014) New Phytol, 204, pp. 474-483
  • Morgan, D., Smith, H., Simulated sunflecks have large, rapid effects on plant stem extension (1978) Nature, 273, pp. 534-536
  • Morgan, D.C., O’Brien, T., Smith, H., Rapid photomodulation of stem extension in light-grown Sinapis alba L.: Studies on kinetics, site of perception and photoreceptor (1980) Planta, 150, pp. 95-101
  • Cole, B., Kay, S.A., Chory, J., Automated analysis of hypocotyl growth dynamics during shade avoidance in Arabidopsis (2011) Plant J, 65, pp. 991-1000
  • Hersch, M., Light intensity modulates the regulatory network of the shade avoidance response in Arabidopsis (2014) Proc Natl Acad Sci USA, 111, pp. 6515-6520
  • Krishna Reddy, S., Finlayson, S.A., Phytochrome B promotes branching in Arabidopsis by suppressing auxin signaling (2014) Plant Physiol, 164, pp. 1542-1550
  • Kunihiro, A., Phytochrome-interacting factor 4 and 5 (PIF4 and PIF5) activate the homeobox ATHB2 and auxin-inducible IAA29 genes in the coincidence mechanism underlying photoperiodic control of plant growth of Arabidopsis thaliana (2011) Plant Cell Physiol, 52, pp. 1315-1329
  • Sun, J., Qi, L., Li, Y., Zhai, Q., Li, C., PIF4 and PIF5 transcription factors link blue light and auxin to regulate the phototropic response in Arabidopsis (2013) Plant Cell, 25, pp. 2102-2114

Citas:

---------- APA ----------
Pucciariello, O., Legris, M., Rojas, C.C., Iglesias, M.J., Hernando, C.E., Dezar, C., Vazquez, M.,..., Casal, J.J. (2018) . Rewiring of auxin signaling under persistent shade. Proceedings of the National Academy of Sciences of the United States of America, 115(21), 5612-5617.
http://dx.doi.org/10.1073/pnas.1721110115
---------- CHICAGO ----------
Pucciariello, O., Legris, M., Rojas, C.C., Iglesias, M.J., Hernando, C.E., Dezar, C., et al. "Rewiring of auxin signaling under persistent shade" . Proceedings of the National Academy of Sciences of the United States of America 115, no. 21 (2018) : 5612-5617.
http://dx.doi.org/10.1073/pnas.1721110115
---------- MLA ----------
Pucciariello, O., Legris, M., Rojas, C.C., Iglesias, M.J., Hernando, C.E., Dezar, C., et al. "Rewiring of auxin signaling under persistent shade" . Proceedings of the National Academy of Sciences of the United States of America, vol. 115, no. 21, 2018, pp. 5612-5617.
http://dx.doi.org/10.1073/pnas.1721110115
---------- VANCOUVER ----------
Pucciariello, O., Legris, M., Rojas, C.C., Iglesias, M.J., Hernando, C.E., Dezar, C., et al. Rewiring of auxin signaling under persistent shade. Proc. Natl. Acad. Sci. U. S. A. 2018;115(21):5612-5617.
http://dx.doi.org/10.1073/pnas.1721110115