Hormone-mediated growth dynamics of the barley pericarp as revealed by magnetic resonance imaging and transcript profiling

. 2015 Nov ; 66 (21) : 6927-43. [epub] 20150814

Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid26276866

The shape of the maternal pericarp affects cereal grain mass and yield. Pericarp growth was analysed by magnetic resonance imaging (MRI), revealing topological maps of mobile water in developing pericarp of barley (Hordeum vulgare) and displaying tissue regions actively elongating in specific temporal-spatial patterns. Correlation analysis of MRI signals and growth rates reveals that growth in length is mediated by dorsal and also lateral rather than ventral regions. Growth in thickness is related to ventral regions. Switching from dorsal to ventral growth is associated with differential expression of axial regulators of the HD-ZipIII and Kanadi/Ettin types, and NPH3 photoreceptors, suggesting light-mediated auxin re-distribution. Auxin increases with the highest levels in the basal pericarp at 6 days after fertilization (DAF), together with transcriptionally up-regulated auxin transport and signalling. Gibberellin biosynthesis is transcriptionally up-regulated only later, and levels of bioactive gibberellins increase from 7 to 13 DAF, with higher levels in ventral than dorsal regions. Differential gene expression related to cell expansion indicates genes related to apoplast acidification, wall relaxation, sugar cleavage, water transport, and cell wall biosynthesis. Candidate genes potentially involved in pericarp extension are distinguished by their temporal expression, representing potential isoforms responsible for dorsal-mediated early growth in length or ventral-mediated late growth in thickness.

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Burton RA, Fincher GB. 2014. Evolution and development of cell walls in cereal grains. Frontiers in Plant Sciences 5, 456. PubMed PMC

Cochrane MP, Duffus CM. 1980. The nucellar projection and modified aleurone in the crease region of developing caryopses of barley (Hordeum vulgare L. var.distichum). Protoplasma 103, 361–375.

Cosgrove DJ. 2000. Expansive growth of plant cell walls. Plant Physiology and Biochemistry 38, 109–124. PubMed

Ferrandiz C, Pelaz S, Yanofsky MF. 1999. Control of carpel and fruit development in Arabidopsis. Annual Review of Biochemistry 68, 321–354. PubMed

Friml J, Vieten A, Sauer M, Weijers D, Schwarz H, Hamann T, Offringa R, Jurgens G. 2003. Efflux-dependent auxin gradients establish the apical–basal axis of Arabidopsis. Nature 426, 147–153. PubMed

Fuchs I, Philippar K, Hedrich R. 2006. Ion channels meet auxin action. Plant Biology (Stuttgart) 8, 353–359. PubMed

Haga K, Takano M, Neumann R, Iino M. 2005. The rice COLEOPTILE PHOTOTROPISM1 gene encoding an ortholog of Arabidopsis NPH3 is required for phototropism of coleoptiles and lateral translocation of auxin. The Plant Cell 17, 103–115. PubMed PMC

Hayashi K. 2012. The interaction and integration of auxin signaling components. Plant and Cell Physiology 53, 965–975. PubMed

Hedden P, Phillips AL. 2000. Gibberellin metabolism: new insights revealed by the genes. Trends in Plant Sciences 5, 523–530. PubMed

Holland JJ, Roberts D, Liscum E. 2009. Understanding phototropism: from Darwin to today. Journal of Experimental Botany 60, 1969–1978. PubMed

Hu J, Mitchum MG, Barnaby N, et al. 2008. Potential sites of bioactive gibberellin production during reproductive growth in Arabidopsis. The Plant Cell 20, 320–336. PubMed PMC

Ilegems M, Douet V, Meylan-Bettex M, Uyttewaal M, Brand L, Bowman JL, Stieger PA. 2010. Interplay of auxin, KANADI and Class III HD-ZIP transcription factors in vascular tissue formation. Development 137, 975–984. PubMed

Ishida N, Koizumi M, Kano H. 1994. Ontogenetic changes in water in cherry tomato fruits measured by nuclear magnetic resonance imaging. Scientia Horticulturae 57, 335–346.

Itoh J, Hibara K, Sato Y, Nagato Y. 2008. Developmental role and auxin responsiveness of Class III homeodomain leucine zipper gene family members in rice. Plant Physiology 147, 1960–1975. PubMed PMC

Ivakov A, Persson S. 2013. Plant cell shape: modulators and measurements. Frontiers in Plant Sciences 4, 439. PubMed PMC

Joyce DC, Hockings PD, Mazucco RA, Shorter AJ. 2002. H-1-Nuclear magnetic resonance imaging of ripening ‘Kensington Pride’ mango fruit. Functional Plant Biology 29, 873–879. PubMed

Kalve S, De Vos D, Beemster GT. 2014. Leaf development: a cellular perspective. Frontiers in Plant Sciences 5, 362. PubMed PMC

Kohl S, Hollmann J, Erban A, Kopka J, Riewe D, Weschke W, Weber H. 2015. Metabolic and transcriptional transitions in barley glumes reveal a role as transitory resource buffers during endosperm filling. Journal of Experimental Botany 66, 1397–1411. PubMed PMC

Kutschera U, Niklas KJ. 2013. Cell division and turgor-driven stem elongation in juvenile plants: a synthesis. Plant Science 207, 45–56. PubMed

Kutschera U, Wang ZY. 2015. Growth-limiting proteins in maize coleoptiles and the auxin–brassinosteroid hypothesis of mesocotyl elongation. Protoplasma doi:10.1007/s00709-015-0787-4. PubMed PMC

Lizana XC, Riegel R, Gomez LD, Herrera J, Isla A, McQueen-Mason SJ, Calderini DF. 2010. Expansins expression is associated with grain size dynamics in wheat (Triticum aestivum L.). Journal of Experimental Botany 61, 1147–1157. PubMed PMC

Ljung K. 2013. Auxin metabolism and homeostasis during plant development. Development 140, 943–950. PubMed

Manz B, Muller K, Kucera B, Volke F, Leubner-Metzger G. 2005. Water uptake and distribution in germinating tobacco seeds investigated in vivo by nuclear magnetic resonance imaging. Plant Physiology 138, 1538–1551. PubMed PMC

Marchant A, Bhalerao R, Casimiro I, Eklof J, Casero PJ, Bennett M, Sandberg G. 2002. AUX1 promotes lateral root formation by facilitating indole-3-acetic acid distribution between sink and source tissues in the Arabidopsis seedling. The Plant Cell 14, 589–597. PubMed PMC

Maurel C, Santoni V, Luu DT, Wudick MM, Verdoucq L. 2009. The cellular dynamics of plant aquaporin expression and functions. Current Opinion in Plant Biology 12, 690–698. PubMed

Metzner R, van Dusschoten D, Buhler J, Schurr U, Jahnke S. 2014. Belowground plant development measured with magnetic resonance imaging (MRI): exploiting the potential for non-invasive trait quantification using sugar beet as a proxy. Frontiers in Plant Sciences 5, 469. PubMed PMC

Pekker I, Alvarez JP, Eshed Y. 2005. Auxin response factors mediate Arabidopsis organ asymmetry via modulation of KANADI activity. The Plant Cell 17, 2899–2910. PubMed PMC

Pěnčík A, Rolcik J, Novak O, Magnus V, Bartak P, Buchtik R, Salopek-Sondi B, Strnad M. 2009. Isolation of novel indole-3-acetic acid conjugates by immunoaffinity extraction. Talanta 80, 651–655. PubMed

Perrot-Rechenmann C. 2010. Cellular responses to auxin: division versus expansion. Cold Spring Harbor Perspectives in Biology 2, a001446. PubMed PMC

Pielot R, Seiffert U, Manz B, Weier D, Volke F, Weschke W. 2008. 4D warping for analysing morphological changes in seed development of barley grains. International Conference on Computer Vision Theory and Applications (VISAPP) , 335–340.

Radchuk VV, Borisjuk L, Sreenivasulu N, Merx K, Mock HP, Rolletschek H, Wobus U, Weschke W. 2009. Spatiotemporal profiling of starch biosynthesis and degradation in the developing barley grain. Plant Physiology 150, 190–204. PubMed PMC

Radchuk V, Weier D, Radchuk R, Weschke W, Weber H. 2011. Development of maternal seed tissue in barley is mediated by regulated cell expansion and cell disintegration and coordinated with endosperm growth. Journal of Experimental Botany 62, 1217–1227. PubMed PMC

Rathjen JR, Strounina EV, Mares DJ. 2009. Water movement into dormant and non-dormant wheat (Triticum aestivum L.) grains. Journal of Experimental Botany 60, 1619–1631. PubMed PMC

Ringli C. 2010. Monitoring the outside: cell wall-sensing mechanisms. Plant Physiology 153, 1445–1452. PubMed PMC

Robinson A, Clark CJ, Clemens J. 2000. Using 1H magnetic resonance imaging and complementary analytical techniques to characterize developmental changes in the Zantedeschia Spreng. tuber. Journal of Experimental Botany 51, 2009–2020. PubMed

Rolletschek H, Weschke W, Weber H, Wobus U, Borisjuk L. 2004. Energy state and its control on seed development: starch accumulation is associated with high ATP and steep oxygen gradients within barley grains. Journal of Experimental Botany 55, 1351–1359. PubMed

Sakai T, Haga K. 2012. Molecular genetic analysis of phototropism in Arabidopsis. Plant and Cell Physiology 53, 1517–1534. PubMed PMC

Scarpella E, Barkoulas M, Tsiantis M. 2010. Control of leaf and vein development by auxin. Cold Spring Harbor Perspectives in Biology 2, a001511. PubMed PMC

Seymour GB, Ostergaard L, Chapman NH, Knapp S, Martin C. 2013. Fruit development and ripening. Annual Review of Plant Biology 64, 219–241. PubMed

Snaar JE, Van As H. 1992. Probing water compartments and membrane permeability in plant cells by H NMR relaxation measurements. Biophysical Journal 63, 1654–1658. PubMed PMC

Stark M, Manz B, Ehlers A, Kuppers M, Riemann I, Volke F, Siebert U, Weschke W, Konig K. 2007. Multiparametric high-resolution imaging of barley embryos by multiphoton microscopy and magnetic resonance micro-imaging. Microscopy Research and Technique 70, 426–432. PubMed

Stepanova AN, Yun J, Robles LM, Novak O, He W, Guo H, Ljung K, Alonso JM. 2011. The Arabidopsis YUCCA1 flavin monooxygenase functions in the indole-3-pyruvic acid branch of auxin biosynthesis. The Plant Cell 23, 3961–3973. PubMed PMC

Swarup R, Peret B. 2012. AUX/LAX family of auxin influx carriers—an overview. Frontiers in Plant Sciences 3, 225. PubMed PMC

Thimm O, Bläsing O, Gibon Y, Nagel A, Meyer S, Krüger P, Selbig J, Müller LA, Rhee SY, Stitt M. 2004. Mapman: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. The Plant Journal 37, 914–939. PubMed

Toga AW, Thompson P. 1999. An introduction to brain warping. In: Toga W, ed. Brain warping . San Diego: Academic Press, 1–26.

Ugarte C, Calderini DF, Slafer GA. 2007. Grain weight and grain number responsiveness to pre-anthesis temperature in wheat, barley and triticale. Field Crops Research 100, 240–248.

Urbanova T, Tarkowska D, Novak O, Hedden P, Strnad M. 2013. Analysis of gibberellins as free acids by ultra performance liquid chromatography-tandem mass spectrometry. Talanta 112, 85–94. PubMed

Van As H. 2007. Intact plant MRI for the study of cell water relations, membrane permeability, cell-to-cell and long distance water transport. Journal of Experimental Botany 58, 743–756. PubMed

van der Weerd L, Claessens MM, Ruttink T, Vergeldt FJ, Schaafsma TJ, Van As H. 2001. Quantitative NMR microscopy of osmotic stress responses in maize and pearl millet. Journal of Experimental Botany 52, 2333–2343. PubMed

Weier D, Thiel J, Kohl S, Tarkowska D, Strnad M, Schaarschmidt S, Weschke W, Weber H, Hause B. 2014. Gibberellin-to-abscisic acid balances govern development and differentiation of the nucellar projection of barley grains. Journal of Experimental Botany 65, 5291–5304. PubMed PMC

Weschke W, Panitz R, Sauer N, Wang Q, Neubohn B, Weber H, Wobus U. 2000. Sucrose transport into barley seeds: molecular characterization of two transporters and implications for seed development and starch accumulation. The Plant Journal 21, 455–467. PubMed

Yamaguchi S. 2008. Gibberellin metabolism and its regulation. Annual Review of Plant Biology 59, 225–251. PubMed

Yooyongwech S, Horigane AK, Yoshida M, Yamaguchi M, Sekozawa Y, Sugaya S, Gemma H. 2008. Changes in aquaporin gene expression and magnetic resonance imaging of water status in peach tree flower buds during dormancy. Physiologia Plantarum 134, 522–533. PubMed

Zažímalová E, Murphy AS, Yang H, Hoyerová K, Hošek P. 2010. Auxin transporters—why so many? Cold Spring Harbor Perspectives in Biology 2, a001552. PubMed PMC

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