دورية أكاديمية
أعرض في EDS

Reduction in organ-organ friction is critical for corolla elongation in morning glory.

التفاصيل البيبلوغرافية
العنوان: Reduction in organ-organ friction is critical for corolla elongation in morning glory.
المؤلفون: Shimoki A; Graduate School of Life and Environmental Sciences, Kyoto Prefectural University, Kyoto, Japan., Tsugawa S; Graduate School of Science and Technology, Nara Institute of Science and Technology, Ikoma, Nara, Japan., Ohashi K; Graduate School of Life and Environmental Sciences, Kyoto Prefectural University, Kyoto, Japan., Toda M; Graduate School of Life and Environmental Sciences, Kyoto Prefectural University, Kyoto, Japan., Maeno A; Plant Resource Development, Division of Genetic Resource Centre, National Institute of Genetics, Shizuoka, Japan., Sakamoto T; Centre for Plant Sciences, Kyoto Sangyo University, Kyoto, Japan., Kimura S; Centre for Plant Sciences, Kyoto Sangyo University, Kyoto, Japan.; Department of Industrial Life Sciences, Faculty of Life Sciences, Kyoto Sangyo University, Kyoto, Japan., Nobusawa T; Graduate School of Integrated Sciences for Life, Hiroshima University, Hiroshima, Japan., Nagao M; Graduate School of Life and Environmental Sciences, Kyoto Prefectural University, Kyoto, Japan., Nitasaka E; Graduate School of Science, Kyushu University, Fukuoka, Japan., Demura T; Graduate School of Science and Technology, Nara Institute of Science and Technology, Ikoma, Nara, Japan., Okada K; Faculty of Agriculture, Ryukoku University, Shiga, Japan., Takeda S; Graduate School of Life and Environmental Sciences, Kyoto Prefectural University, Kyoto, Japan. seijitakeda@kpu.ac.jp.; Biotechnology Research Department, Kyoto Prefectural Agriculture Forestry and Fisheries Technology Centre, Kyoto, Japan. seijitakeda@kpu.ac.jp.
المصدر: Communications biology [Commun Biol] 2021 Mar 05; Vol. 4 (1), pp. 285. Date of Electronic Publication: 2021 Mar 05.
نوع المنشور: Journal Article; Research Support, Non-U.S. Gov't; Video-Audio Media
اللغة: English
بيانات الدورية: Publisher: Nature Publishing Group UK Country of Publication: England NLM ID: 101719179 Publication Model: Electronic Cited Medium: Internet ISSN: 2399-3642 (Electronic) Linking ISSN: 23993642 NLM ISO Abbreviation: Commun Biol Subsets: MEDLINE
أسماء مطبوعة: Original Publication: London, United Kingdom : Nature Publishing Group UK, [2018]-
مواضيع طبية MeSH: Plant Development*, Flowers/*growth & development , Ipomoea nil/*growth & development , Plants, Genetically Modified/*growth & development , Trichomes/*growth & development, Computer Simulation ; Flowers/genetics ; Friction ; Ipomoea nil/genetics ; Models, Biological ; Mutation ; Plants, Genetically Modified/genetics ; Stress, Mechanical ; Trichomes/genetics
مستخلص: In complex structures such as flowers, organ-organ interactions are critical for morphogenesis. The corolla plays a central role in attracting pollinators: thus, its proper development is important in nature, agriculture, and horticulture. Although the intraorgan mechanism of corolla development has been studied, the importance of organ-organ interactions during development remains unknown. Here, using corolla mutants of morning glory described approximately 200 years ago, we show that glandular secretory trichomes (GSTs) regulate floral organ interactions needed for corolla morphogenesis. Defects in GST development in perianth organs result in folding of the corolla tube, and release of mechanical stress by sepal removal restores corolla elongation. Computational modeling shows that the folding occurs because of buckling caused by mechanical stress from friction at the distal side of the corolla. Our results suggest a novel function of GSTs in regulating the physical interaction of floral organs for macroscopic morphogenesis of the corolla.
References: Scheres, B. Plant cell identity. The role of position and lineage. Plant Physiol. 125, 112–114 (2001). (PMID: 11154310153933910.1104/pp.125.1.112)
Pallakies, H. & Simon, R. in Encyclopedia of Life Sciences (ELS) (John Wiley & Sons, Ltd.) https://doi.org/10.1002/9780470015902.a0002069.pub2 (2010).
Krizek, B. A. & Fletcher, J. C. Molecular mechanisms of flower development: an armchair guide. Nat. Rev. Genet. 6, 688–698 (2005). (PMID: 1615137410.1038/nrg1675)
Coen, E. S. & Meyerowitz, E. M. The war of the whorls: genetic interactions controlling flower development. Nature 353, 31–37 (1991). (PMID: 171552010.1038/353031a0)
Kanno, A. Molecular mechanism regulating floral architecture in monocotyledonous ornamental plants. Hort. J. 85, 8–22 (2016). (PMID: 10.2503/hortj.MI-IR05)
Raczynska-Szajgin, M. & Nakielski, J. Growth and cellular patterns in the petal epidermis of Antirrhinum majus: empirical studies. Ann. Bot. 113, 403–416 (2014). (PMID: 2425228210.1093/aob/mct263)
Rolland-Lagan, A. G., Bangham, J. A. & Coen, E. Growth dynamics underlying petal shape and asymmetry. Nature 422, 161–163 (2003). (PMID: 1263478510.1038/nature01443)
Huang, C., Wang, Z., Quinn, D., Suresh, S. & Hsia, K. J. Differential growth and shape formation in plant organs. Proc. Natl. Acad. Sci. USA 115, 12359–12364 (2018). (PMID: 3045531110.1073/pnas.18112961156298086)
Park, K. I. et al. A bHLH regulatory gene in the common morning glory, Ipomoea purpurea, controls anthocyanin biosynthesis in flowers, proanthocyanidin and phytomelanin pigmentation in seeds, and seed trichome formation. Plant J. 49, 641–654 (2007). (PMID: 1727001310.1111/j.1365-313X.2006.02988.x)
Inagaki, Y., Hisatomi, Y., Suzuki, T., Kasahara, K. & Iida, S. Isolation of a Suppressor-mutator/Enhancer-like transposable element, Tpn1, from Japanese morning glory bearing variegated flowers. Plant Cell 6, 375–383 (1994). (PMID: 8180498160440)
Nitasaka, E. Insertion of an En/Spm-related transposable element into a floral homeotic gene DUPLICATED causes a double flower phenotype in the Japanese morning glory. Plant J. 36, 522–531 (2003). (PMID: 1461708210.1046/j.1365-313X.2003.01896.x)
Iwasaki, M. & Nitasaka, E. The FEATHERED gene is required for polarity establishment in lateral organs especially flowers of the Japanese morning glory (Ipomoea nil). Plant Mol. Biol. 62, 913–925 (2006). (PMID: 1697216610.1007/s11103-006-9066-2)
Fukada-Tanaka, S., Inagaki, Y., Yamaguchi, T. & Iida, S. Simplified transposon display (STD): a new prodecure for isolation of a gene tagged by a transposable element belonging to the Tpn1 family in the Japanese morning glory. Plant Biotech. 18, 143–149 (2001). (PMID: 10.5511/plantbiotechnology.18.143)
Hoshino, A. et al. Genome sequence and analysis of the Japanese morning glory Ipomoea nil. Nat. Commun. 7, 13295 (2016). (PMID: 27824041510517210.1038/ncomms13295)
Kotendo, S. Kadan Asagao Tsu https://doi.org/10.11501/2557561 (1815).
Miyake, K. & Imai, Y. On the double flowers of the Japanese morning glory. J. Genet. 19, 97–130 (1927). (PMID: 10.1007/BF02983119)
Imai, Y. The genes of the Japanese morning glory. Jpn. J. Genet. 14, 24–33 (1938). (PMID: 10.1266/jjg.14.24)
Nitasaka, E. Henka Asagao Zukan. ISBN 978-4-7598-1573-3 (2014).
Gere, J. M., Goodno, B. J. Mechanics of Materials 8th edn (2012).
Varner, V. D. & Nelson, C. M. Cellular and physical mechanisms of branching morphogenesis. Development 141, 2750–2759 (2014). (PMID: 25005470419761510.1242/dev.104794)
Simmons, A. T. & Guur, G. M. Trichomes of Lycopersicon species and their hybrids: effects on pests and natural enemies. Agric. For. Entomol. 7, 265–276 (2005). (PMID: 10.1111/j.1461-9555.2005.00271.x)
Tissier, A. Glandular trichomes: what comes after expressed sequence tags? Plant J. 70, 51–68 (2012). (PMID: 2244904310.1111/j.1365-313X.2012.04913.x)
Schilmiller, A. L., Last, R. L. & Pichersky, E. Harnessing plant trichome biochemistry for the production of useful compounds. Plant J. 54, 702–711 (2008). (PMID: 1847687310.1111/j.1365-313X.2008.03432.x)
Asai, T., Hara, N. & Fujimoto, Y. Fatty acid derivatives and dammarane triterpenes from the glandular trichome exudates of Ibicella lutea and Proboscidea louisiana. Phytochemistry 71, 877–894 (2010). (PMID: 2038182110.1016/j.phytochem.2010.02.013)
Ascensao, L. & Pais, M. S. S. Glandular trichomes of Artemisia campestris (ssp. Maritima): ontogeny and histochemistry of the secretory product. Bot. Gaz. 148, 221–227 (1987). (PMID: 10.1086/337650)
Gonzalez, A., Zhao, M., Leavitt, J. M. & Lloyd, A. M. Regulation of the anthocyanin biosynthetic pathway by the TTG1/bHLH/Myb transcriptional complex in Arabidopsis seedlings. Plant J. 53, 814–827 (2008). (PMID: 1803619710.1111/j.1365-313X.2007.03373.x)
Dubos, C. et al. MYB transcription factors in Arabidopsis. Trends Plant Sci. 15, 573–581 (2010). (PMID: 2067446510.1016/j.tplants.2010.06.005)
Chezem, W. R. & Clay, N. K. Regulation of plant secondary metabolism and associated specialized cell development by MYBs and bHLHs. Phytochemistry 131, 26–43 (2016). (PMID: 27569707504860110.1016/j.phytochem.2016.08.006)
Stracke, R., Werber, M. & Weisshaar, B. The R2R3-MYB gene family in Arabidopsis thaliana. Curr. Opin. Plant Biol. 4, 447–456 (2001). (PMID: 1159750410.1016/S1369-5266(00)00199-0)
Heim, M. A. et al. The basic helix-loop-helix transcription factor family in plants: a genome-wide study of protein structure and functional diversity. Mol. Biol. Evol. 20, 735–747 (2003). (PMID: 1267953410.1093/molbev/msg088)
Bailey, P. C. et al. Update on the basic helix-loop-helix transcription factor gene family in Arabidopsis thaliana. Plant Cell 15, 2497–2502 (2003). (PMID: 1460021154026710.1105/tpc.151140)
Matias-Hernandez, L. et al. AaMYB1 and its orthologue AtMYB61 affect terpene metabolism and trichome development in Artemisia annua and Arabidopsis thaliana. Plant J. 90, 520–534 (2017). (PMID: 2820797410.1111/tpj.13509)
Chalvin, C., Drevensek, S., Dron, M., Bendahmane, A. & Boualem, A. Genetic control of glandular trichome development. Trends Plant Sci. 25, 477–487 (2020). (PMID: 3198361910.1016/j.tplants.2019.12.025)
Tian, N. et al. The molecular basis of glandular trichome development and secondary metabolism in plants. Plant Gene 12, 1–12 (2017). (PMID: 10.1016/j.plgene.2017.05.010)
Takeda, S. et al. Physical interaction of floral organs controls petal morphogenesis in Arabidopsis. Plant Physiol. 161, 1242–1250 (2013). (PMID: 23314942358559310.1104/pp.112.212084)
Takeda, S., Iwasaki, A., Tatematsu, K. & Okada, K. The Half-Size ABC. Transporter FOLDED PETALS 2/ABCG13 is involved in petal elongation through narrow spaces in Arabidopsis thaliana floral buds. Plants 3, 348–358 (2014). (PMID: 27135508484435110.3390/plants3030348)
Bell, A. D. Plant Form: An Illustrated Guide To Flowering Plant Morphology, New Edition (Timber Press, Inc., 2008).
Wang, H., Olofsson, L., Lundgren, A. & Brodelius, P. E. Trichome-specific expression of amorpha-4,11-diene synthase, a key enzyme of artemisinin biosynthesis in Artemisia annua L., as reported by a promoter-GUS fusion. Am. J. Plant Sci. 02, 619–628 (2011). (PMID: 10.4236/ajps.2011.24073)
Wang, H., Han, J., Kanagarajan, S., Lundgren, A. & Brodelius, P. E. Studies on the expression of sesquiterpene synthases using promoter-beta-glucuronidase fusions in transgenic Artemisia annua L. PLoS ONE 8, e80643 (2013). (PMID: 24278301383840810.1371/journal.pone.0080643)
Spyropoulou, E. A., Haring, M. A. & Schuurink, R. C. Expression of Terpenoids 1, a glandular trichome-specific transcription factor from tomato that activates the terpene synthase 5 promoter. Plant Mol. Biol. 84, 345–357 (2014). (PMID: 2414238210.1007/s11103-013-0142-0)
Shangguan, X. X., Xu, B., Yu, Z. X., Wang, L. J. & Chen, X. Y. Promoter of a cotton fibre MYB gene functional in trichomes of Arabidopsis and glandular trichomes of tobacco. J. Exp. Bot. 59, 3533–3542 (2008). (PMID: 18711121256115810.1093/jxb/ern204)
Jindal, S., Longchar, B., Singh, A. & Gupta, V. Promoters of AaGL2 and AaMIXTA-Like1 genes of Artemisia annua direct reporter gene expression in glandular and non-glandular trichomes. Plant Signal. Behav. 10, e1087629 (2015). (PMID: 26340695485434710.1080/15592324.2015.1087629)
Hamant, O. & Saunders, T. E. Shaping organs: shared structural principles across kingdoms. Annu. Rev. Cell Dev. Biol. https://doi.org/10.1146/annurev-cellbio-012820-103850 (2020).
Metscher, B. D. MicroCT for comparative morphology: simple staining methods allow high-contrast 3D imaging of diverse non-mineralized animal tissues. BMC Physiol. 9, 11 (2009). (PMID: 19545439271791110.1186/1472-6793-9-11)
Staedler, Y. M., Masson, D. & Schonenberger, J. Plant tissues in 3D via X-ray tomography: simple contrasting methods allow high resolution imaging. PLoS ONE 8, e75295 (2013). (PMID: 24086499378551510.1371/journal.pone.0075295)
Degenhardt, K., Wright, A. C., Horng, D., Padmanabhan, A. & Epstein, J. A. Rapid 3D phenotyping of cardiovascular development in mouse embryos by micro-CT with iodine staining. Circ. Cardiovasc. Imaging 3, 314–322 (2010). (PMID: 20190279305989210.1161/CIRCIMAGING.109.918482)
Tsuda, K. et al. KNOTTED1 Cofactors, BLH12 and BLH14, regulate internode patterning and vein anastomosis in maize. Plant Cell 29, 1105–1118 (2017). (PMID: 28381444546603110.1105/tpc.16.00967)
Hervieux, N. et al. A mechanical feedback restricts sepal growth and shape in Arabidopsis. Curr. Biol. S0960–9822, 30180–30184 (2016).
Hervieux, N. et al. Mechanical shielding of rapidly growing cells buffers growth heterogeneity and contributes to organ shape reproducibility. Curr. Biol. 27, 3468–3479.e3464 (2017). (PMID: 2912953410.1016/j.cub.2017.10.033)
Hong, L. et al. Variable cell growth yields reproducible organ development through spatiotemporal averaging. Dev. Cell 38, 15–32 (2016). (PMID: 2740435610.1016/j.devcel.2016.06.016)
Tsugawa, S. Suppression of soft spots and excited modes in the shape deformation model with spatio-temporal growth noise. J. Theor. Biol. 486, 110092 (2020). (PMID: 3177053710.1016/j.jtbi.2019.110092)
Hecht, F. New development in freefem++. J. Numer. Math. 20, 251–265 (2012). (PMID: 10.1515/jnum-2012-0013)
Bligh, E. G. & Dyer, W. J. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911–917 (1959). (PMID: 1367137810.1139/y59-099)
Brunner, A. M., Yakovlev, I. A. & Strauss, S. H. Validating internal controls for quantitative plant gene expression studies. BMC Plant Biol. 4, 14 (2004). (PMID: 1531765551530110.1186/1471-2229-4-14)
Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754–1760 (2009). (PMID: 19451168270523410.1093/bioinformatics/btp324)
Robinson, M. D., McCarthy, D. J. & Smyth, G. K. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139–140 (2010). (PMID: 1991030810.1093/bioinformatics/btp616)
Mi, H., Muruganujan, A., Ebert, D., Huang, X. & Thomas, P. D. PANTHER version 14: more genomes, a new PANTHER GO-slim and improvements in enrichment analysis tools. Nucleic Acids Res. 47, D419–D426 (2019). (PMID: 3040759410.1093/nar/gky1038)
تواريخ الأحداث: Date Created: 20210306 Date Completed: 20210810 Latest Revision: 20230130
رمز التحديث: 20230130
مُعرف محوري في PubMed: PMC7935917
DOI: 10.1038/s42003-021-01814-x
PMID: 33674689
قاعدة البيانات: MEDLINE
الوصف
تدمد:2399-3642
DOI:10.1038/s42003-021-01814-x