Molecular Communication for Coordinated Seed and Fruit Development: What Can We Learn from Auxin and Sugars?

. 2019 Feb 21 ; 20 (4) : . [epub] 20190221

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články, přehledy

Perzistentní odkaz   https://www.medvik.cz/link/pmid30795528

Grantová podpora
CZ.02.1.01/0.0/0.0/16_019/0000738 Ministerstvo Školství, Mládeže a Tělovýchovy

Seed development in flowering plants is a critical part of plant life for successful reproduction. The formation of viable seeds requires the synchronous growth and development of the fruit and the three seed structures: the embryo, the endosperm, the seed coat. Molecular communication between these tissues is crucial to coordinate these developmental processes. The phytohormone auxin is a significant player in embryo, seed and fruit development. Its regulated local biosynthesis and its cell-to-cell transport capacity make of auxin the perfect candidate as a signaling molecule to coordinate the growth and development of the embryo, endosperm, seed and fruit. Moreover, newly formed seeds need nutrients and form new carbon sink, generating high sugar flow from vegetative tissues to the seeds. This review will discuss how auxin and sugars may be considered as signaling molecules to coordinate seed and fruit development.

Zobrazit více v PubMed

Dorcey E., Urbez C., Blázquez M.A., Carbonell J., Perez-Amador M.A. Fertilization-dependent auxin response in ovules triggers fruit development through the modulation of gibberellin metabolism in Arabidopsis. Plant J. 2009;58:318–332. doi: 10.1111/j.1365-313X.2008.03781.x. PubMed DOI

Cucinotta M., Manrique S., Cuesta C., Benková E., Novak O., Colombo L.L. CUP-SHAPED COTYLEDON1 (CUC1) and CUC2 regulate cytokinin homeostasis to determine ovule number in Arabidopsis. J. Exp. Bot. 2018;69:5169–5176. doi: 10.1093/jxb/ery281. PubMed DOI PMC

Cucinotta M., Manrique S., Guazzotti A., Quadrelli N.E., Mendes M.A., Benková E., Colombo L.L. Cytokinin response factors integrate auxin and cytokinin pathways for female reproductive organ development. Development. 2016;143:4419–4424. doi: 10.1242/dev.143545. PubMed DOI

Gómez M.D., Barro-Trastoy D., Escoms E., Saura-Sánchez M., Sánchez I., Briones-Moreno A., Vera-Sirera F., Carrera E., Ripoll J.J., Yanofsky M.F., et al. Gibberellins negatively modulate ovule number in plants. Development. 2018;145:dev163865. doi: 10.1242/dev.163865. PubMed DOI PMC

Galván-Ampudia C.S., Cerutti G., Legrand J., Azais R., Brunoud G., Moussu S., Wenzl C., Lohmann J.U., Godin C.C., Vernoux T. From spatio-temporal morphogenetic gradients to rhythmic patterning at the shoot apex. bioRxiv. 2019 doi: 10.1101/469718. DOI

Wybouw B., De Rybel B. Cytokinin—A Developing Story. Trends Plant Sci. 2019;24:177–185. doi: 10.1016/j.tplants.2018.10.012. PubMed DOI

Robert H.S., Khaitova L.C., Mroue S., Benková E. The importance of localized auxin production for morphogenesis of reproductive organs and embryos in Arabidopsis. J. Exp. Bot. 2015;66:5029–5042. doi: 10.1093/jxb/erv256. PubMed DOI

Joldersma D., Liu Z. The making of virgin fruit: The molecular and genetic basis of parthenocarpy. J. Exp. Bot. 2018;69:955–962. doi: 10.1093/jxb/erx446. PubMed DOI PMC

Stepanova A.N., Yun J.J., Robles L.M., Novak O., He W., Guo H., Ljung K., Alonso J.M. The Arabidopsis YUCCA1 flavin monooxygenase functions in the indole-3-pyruvic acid branch of auxin biosynthesis. Plant Cell. 2011;23:3961–3973. doi: 10.1105/tpc.111.088047. PubMed DOI PMC

Mashiguchi K., Tanaka K., Sakai T., Sugawara S., Kawaide H., Natsume M., Hanada A., Yaeno T., Shirasu K., Yao H., et al. The main auxin biosynthesis pathway in Arabidopsis. Proc. Natl. Acad. Sci. USA. 2011;108:18512–18517. doi: 10.1073/pnas.1108434108. PubMed DOI PMC

Won C., Shen X., Mashiguchi K., Zheng Z., Dai X., Cheng Y., Kasahara H., Kamiya Y., Chory J., Zhao Y. Conversion of tryptophan to indole-3-acetic acid by TRYPTOPHAN AMINOTRANSFERASES OF ARABIDOPSIS and YUCCAs in Arabidopsis. Proc. Natl. Acad. Sci. USA. 2011;108:18518–18523. doi: 10.1073/pnas.1108436108. PubMed DOI PMC

Stepanova A.N., Robertson-Hoyt J., Yun J.J., Benavente L.M., Xie D.-Y., Dolezal K., Schlereth A., Juergens G., Alonso J. M TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell. 2008;133:177–191. doi: 10.1016/j.cell.2008.01.047. PubMed DOI

Zhao Y. Auxin biosynthesis. Arab. Book. 2014;12:e0173. doi: 10.1199/tab.0173. PubMed DOI PMC

Figueiredo D.D., Batista R.A., Roszak P.J., Köhler C.C. Auxin production couples endosperm development to fertilization. Nat. Plants. 2015;1:15184. doi: 10.1038/nplants.2015.184. PubMed DOI

Figueiredo D.D., Batista R.A., Roszak P.J., Hennig L., Köhler C.C. Auxin production in the endosperm drives seed coat development in Arabidopsis. eLife. 2016;5:e20542. doi: 10.7554/eLife.20542. PubMed DOI PMC

Robert H.S., Grones P., Stepanova A.N., Robles L.M., Lokerse A.S., Alonso J.M., Weijers D., Friml J. Local auxin sources orient the apical-basal axis in Arabidopsis embryos. Curr. Biol. 2013;23:2506–2512. doi: 10.1016/j.cub.2013.09.039. PubMed DOI

Robert H.S., Park C., Gutièrrez C.L., Wójcikowska B., Pencík A., Novak O., Chen J., Grunewald W., Dresselhaus T., Friml J., et al. Maternal auxin supply contributes to early embryo patterning in Arabidopsis. Nat. Plants. 2018;4:548–553. doi: 10.1038/s41477-018-0204-z. PubMed DOI PMC

Brumos J., Robles L.M., Yun J.J., Vu T.C., Jackson S., Alonso J.M., Stepanova A.N. Local Auxin Biosynthesis Is a Key Regulator of Plant Development. Dev. Cell. 2018;47:306–318.e5. doi: 10.1016/j.devcel.2018.09.022. PubMed DOI

Cheng Y., Dai X., Zhao Y. Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis. Genes Dev. 2006;20:1790–1799. doi: 10.1101/gad.1415106. PubMed DOI PMC

Cheng Y., Dai X., Zhao Y. Auxin synthesized by the YUCCA flavin monooxygenases is essential for embryogenesis and leaf formation in Arabidopsis. Plant. Cell. 2007;19:2430–2439. doi: 10.1105/tpc.107.053009. PubMed DOI PMC

Chen Q., Dai X., DePaoli H.C., Cheng Y., Takebayashi Y., Kasahara H., Kamiya Y., Zhao Y. Auxin Overproduction in Shoots Cannot Rescue Auxin Deficiencies in Arabidopsis Roots. Plant. Cell Physiol. 2014;55:1072–1079. doi: 10.1093/pcp/pcu039. PubMed DOI PMC

Benková E., Michniewicz M., Sauer M., Teichmann T.T., Seifertová D., Juergens G., Friml J. Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell. 2003;115:591–602. doi: 10.1016/S0092-8674(03)00924-3. PubMed DOI

Adamowski M., Friml J. PIN-Dependent Auxin Transport: Action, Regulation, and Evolution. Plant Cell. 2015;27:20–32. doi: 10.1105/tpc.114.134874. PubMed DOI PMC

Park J., Lee Y., Martinoia E., Geisler M. Plant hormone transporters: What we know and what we would like to know. BMC Biol. 2017;15:93. doi: 10.1186/s12915-017-0443-x. PubMed DOI PMC

Péret B., Swarup K., Ferguson A., Seth M., Yang Y., Dhondt S., James N., Casimiro I., Perry P., Syed A., et al. AUX/LAX genes encode a family of auxin influx transporters that perform distinct functions during Arabidopsis development. Plant Cell. 2012;24:2874–2885. doi: 10.1105/tpc.112.097766. PubMed DOI PMC

Weijers D., Wagner D. Transcriptional Responses to the Auxin Hormone. Annu. Rev. Plant Biol. 2016;67:539–574. doi: 10.1146/annurev-arplant-043015-112122. PubMed DOI

Liao C.-Y., Smet W., Brunoud G., Yoshida S., Vernoux T., Weijers D. Reporters for sensitive and quantitative measurement of auxin response. Nat. Methods. 2015;12:207–210. doi: 10.1038/nmeth.3279. PubMed DOI PMC

Brunoud G., Wells D.M., Oliva M., Larrieu A., Mirabet V., Burrow A.H., Beeckman T., Kepinski S., Traas J., Bennett M.J., et al. A novel sensor to map auxin response and distribution at high spatio-temporal resolution. Nature. 2012;482:103–106. doi: 10.1038/nature10791. PubMed DOI

Ulmasov T., Murfett J., Hagen G., Guilfoyle T.J. Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell. 1997;9:1963–1971. doi: 10.1105/tpc.9.11.1963. PubMed DOI PMC

Christensen C.A., King E.J., Jordan J., Drews G.N. Megagametogenesis in Arabidopsis wild type and the Gf mutant. Sex. Plant Reprod. 1997;10:49–64. doi: 10.1007/s004970050067. DOI

Drews G.N., Yadegari R. Development and function of the angiosperm female gametophyte. Annu. Rev. Genet. 2002;36:99–124. doi: 10.1146/annurev.genet.36.040102.131941. PubMed DOI

Bencivenga S., Colombo L.L., Masiero S. Cross talk between the sporophyte and the megagametophyte during ovule development. Sex. Plant. Reprod. 2011;24:113–121. doi: 10.1007/s00497-011-0162-3. PubMed DOI

Lau S.S., Slane D., Herud O., Kong J., Juergens G. Early embryogenesis in flowering plants: Setting up the basic body pattern. Annu. Rev. Plant. Biol. 2012;63:483–506. doi: 10.1146/annurev-arplant-042811-105507. PubMed DOI

Larsson E., Franks R.G., Sundberg E. Auxin and the Arabidopsis thaliana gynoecium. J. Exp. Bot. 2013;64:2619–2627. doi: 10.1093/jxb/ert099. PubMed DOI

Moubayidin L.L., Østergaard L. Gynoecium formation: An intimate and complicated relationship. Curr. Opin. Gen. Dev. 2017;45:15–21. doi: 10.1016/j.gde.2017.02.005. PubMed DOI

Figueiredo D.D., Köhler C.C. Auxin: A molecular trigger of seed development. Genes Dev. 2018;32:479–490. doi: 10.1101/gad.312546.118. PubMed DOI PMC

Vivian-Smith A., Koltunow A.M. Genetic analysis of growth-regulator-induced parthenocarpy in Arabidopsis. Plant Physiol. 1999;121:437–451. doi: 10.1104/pp.121.2.437. PubMed DOI PMC

Larsson E., Vivian-Smith A., Offringa R., Sundberg E. Auxin homeostasis in Arabidopsis ovules Is anther-dependent at maturation and changes dynamically upon fertilization. Front. Plant Sci. 2017;8:1735. doi: 10.3389/fpls.2017.01735. PubMed DOI PMC

Lituiev D.S., Krohn N.G., Müller B., Jackson D.P., Hellriegel B., Dresselhaus T., Grossniklaus U. Theoretical and experimental evidence indicates that there is no detectable auxin gradient in the angiosperm female gametophyte. Development. 2013;140:4544–4553. doi: 10.1242/dev.098301. PubMed DOI

Panoli A., Martin M.V., Alandete-Saez M., Simon M.K., Neff C., Swarup R., Bellido A., Yuan L., Pagnussat G.C., Sundaresan V. Auxin Import and Local Auxin Biosynthesis Are Required for Mitotic Divisions, Cell Expansion and Cell Specification during Female Gametophyte Development in Arabidopsis thaliana. PLoS ONE. 2015;10:e0126164. doi: 10.1371/journal.pone.0126164. PubMed DOI PMC

Mozgova I., Köhler C.C., Hennig L. Keeping the gate closed: Functions of the polycomb repressive complex PRC2 in development. Plant J. 2015;83:121–132. doi: 10.1111/tpj.12828. PubMed DOI

Mravec J., Kubes M., Bielach A., Gaykova V., Petrásek J., Skůpa P., Chand S., Benková E., Zazímalová E., Friml J. Interaction of PIN and PGP transport mechanisms in auxin distribution-dependent development. Development. 2008;135:3345–3354. doi: 10.1242/dev.021071. PubMed DOI

Forestan C., Meda S., Varotto S. ZmPIN1-Mediated Auxin Transport Is Related to Cellular Differentiation during Maize Embryogenesis and Endosperm Development. Plant Physiol. 2010;152:1373–1390. doi: 10.1104/pp.109.150193. PubMed DOI PMC

Bernardi J., Lanubile A., Li Q.-B., Kumar D., Kladnik A., Cook S.D., Ross J.J., Marocco A., Chourey P.S. Impaired Auxin Biosynthesis in the defective endosperm18 Mutant Is Due to Mutational Loss of Expression in the ZmYuc1 Gene Encoding Endosperm-Specific YUCCA1 Protein in Maize. Plant Physiol. 2012;160:1318–1328. doi: 10.1104/pp.112.204743. PubMed DOI PMC

Locascio A., Roig-Villanova I., Bernardi J., Varotto S. Current perspectives on the hormonal control of seed development in Arabidopsis and maize: A focus on auxin. Front. Plant. Sci. 2014;5:412. doi: 10.3389/fpls.2014.00412. PubMed DOI PMC

Bernardi J., Li Q.-B., Gao Y., Zhao Y., Battaglia R., Marocco A., Chourey P.S. The Auxin-Deficient Defective Kernel18 (dek18) Mutation Alters the Expression of Seed-Specific Biosynthetic Genes in Maize. J. Plant Growth Regul. 2016;35:770–777. doi: 10.1007/s00344-016-9581-6. DOI

Chen J., Lausser A., Dresselhaus T. Hormonal responses during early embryogenesis in maize. Biochem. Soc. Trans. 2014;42:325–331. doi: 10.1042/BST20130260. PubMed DOI

Robert H.S., Friml J. Auxin and other signals on the move in plants. Nat. Chem. Biol. 2009;5:325–332. doi: 10.1038/nchembio.170. PubMed DOI

Stadler R., Lauterbach C., Sauer N. Cell-to-cell movement of green fluorescent protein reveals post-phloem transport in the outer integument and identifies symplastic domains in Arabidopsis seeds and embryos. Plant Physiol. 2005;139:701–712. doi: 10.1104/pp.105.065607. PubMed DOI PMC

Kawashima T., Goldberg R.B. The suspensor: Not just suspending the embryo. Trends Plant Sci. 2010;15:23–30. doi: 10.1016/j.tplants.2009.11.002. PubMed DOI

Yeung E.C. Embryogeny of Phaseolus: The Role of the Suspensor. Z. Für Pflanzenphysiol. 1980;96:17–28. doi: 10.1016/S0044-328X(80)80096-1. DOI

Nagl W. Translocation of Putrescine in the Ovule, Suspensor and Embryo of Phaseolus coccineus. J. Plant. Physiol. 1990;136:587–591. doi: 10.1016/S0176-1617(11)80218-X. DOI

Creff A., Brocard L., Joubes J., Taconnat L., Doll N.M., Pascal S., Galletti R., Marsollier A.-C., Moussu S., Widiez T., et al. A stress-response-related inter-compartmental signalling pathway regulates embryonic cuticle integrity in Arabidopsis. bioRxiv. 2018:477109-35. doi: 10.1101/477109. PubMed DOI PMC

Ingram G.C. Family life at close quarters: Communication and constraint in angiosperm seed development. Protoplasma. 2010;247:195–214. doi: 10.1007/s00709-010-0184-y. PubMed DOI

Moussu S., Doll N.M., Chamot S., Brocard L., Creff A., Fourquin C., Widiez T., Nimchuk Z.L., Ingram G.C. ZHOUPI and KERBEROS Mediate Embryo/Endosperm Separation by Promoting the Formation of an Extracuticular Sheath at the Embryo Surface. Plant Cell. 2017;29:1642–1656. doi: 10.1105/tpc.17.00016. PubMed DOI PMC

Morley-Smith E.R., Pike M.J., Findlay K., Köckenberger W., Hill L.M., Smith A., Rawsthorne S. The transport of sugars to developing embryos is not via the bulk endosperm in oilseed rape seeds. Plant Physiol. 2008;147:2121–2130. doi: 10.1104/pp.108.124644. PubMed DOI PMC

Chen L.-Q., Lin I.W., Qu X.-Q., Sosso D., McFarlane H.E., Londoño A., Samuels A.L., Frommer W.B. A cascade of sequentially expressed sucrose transporters in the seed coat and endosperm provides nutrition for the Arabidopsis embryo. Plant Cell. 2015;27:607–619. doi: 10.1105/tpc.114.134585. PubMed DOI PMC

Baud S., Wuillème S., Lemoine R., Kronenberger J., Caboche M., Lepiniec L., Rochat C. The AtSUC5 sucrose transporter specifically expressed in the endosperm is involved in early seed development in Arabidopsis. Plant J. 2005;43:824–836. doi: 10.1111/j.1365-313X.2005.02496.x. PubMed DOI

Aguirre M., Kiegle E., Leo G., Ezquer I. Carbohydrate reserves and seed development: An overview. Plant Reprod. 2018;31:263–290. doi: 10.1007/s00497-018-0336-3. PubMed DOI

Durand M., Mainson D., Porcheron B., Maurousset L., Lemoine R., Pourtau N. Carbon source-sink relationship in Arabidopsis thaliana: The role of sucrose transporters. Planta. 2018;247:587–611. doi: 10.1007/s00425-017-2807-4. PubMed DOI PMC

Chen L.-Q., Qu X.-Q., Hou B.-H., Sosso D., Osorio S.S., Fernie A.R., Frommer W.B. Sucrose Efflux Mediated by SWEET Proteins as a Key Step for Phloem Transport. Science. 2012;335:207–211. doi: 10.1126/science.1213351. PubMed DOI

Sauer N. Molecular physiology of higher plant sucrose transporters. FEBS Lett. 2007;581:2309–2317. doi: 10.1016/j.febslet.2007.03.048. PubMed DOI

Wang L., Ruan Y.-L. New insights into roles of cell wall invertase in early seed development revealed by comprehensive spatial and temporal expression patterns of GhCWIN1 in cotton. Plant Physiol. 2012;160:777–787. doi: 10.1104/pp.112.203893. PubMed DOI PMC

Wang L., Ruan Y.-L. Regulation of cell division and expansion by sugar and auxin signaling. Front. Plant Sci. 2013;4:163. doi: 10.3389/fpls.2013.00163. PubMed DOI PMC

Baud S., Boutin J.-P., Miquel M., Lepiniec L., Rochat C. An integrated overview of seed development in Arabidopsis thaliana ecotype WS. Plant Physiol. Biochem. 2002;40:151–160. doi: 10.1016/S0981-9428(01)01350-X. DOI

Hehenberger E.E., Kradolfer D.D., Köhler C.C. Endosperm cellularization defines an important developmental transition for embryo development. Development. 2012;139:2031–2039. doi: 10.1242/dev.077057. PubMed DOI

Serrani J.C., Ruiz-Rivero O., Fos M., García-Martínez J.L. Auxin-induced fruit-set in tomato is mediated in part by gibberellins. Plant J. 2008;56:922–934. doi: 10.1111/j.1365-313X.2008.03654.x. PubMed DOI

Ozga J.A., Reinecke D.M., Ayele B.T., Ngo P., Nadeau C., Wickramarathna A.D. Developmental and Hormonal Regulation of Gibberellin Biosynthesis and Catabolism in Pea Fruit. Plant Physiol. 2009;150:448–462. doi: 10.1104/pp.108.132027. PubMed DOI PMC

Hu Y., Zhou L., Huang M., He X., Yang Y., Liu X., Li Y., Hou X. Gibberellins play an essential role in late embryogenesis of Arabidopsis. Nat. Plants. 2018;4:289–298. doi: 10.1038/s41477-018-0143-8. PubMed DOI

Fuentes S., Ljung K., Sorefan K., Alvey E., Harberd N.P., Østergaard L. Fruit growth in Arabidopsis occurs via DELLA-dependent and DELLA-independent gibberellin responses. Plant Cell. 2012;24:3982–3996. doi: 10.1105/tpc.112.103192. PubMed DOI PMC

Rieu I., Eriksson S., Powers S.J., Gong F., Griffiths J., Woolley L., Benlloch R., Nilsson O., Thomas S.G., Hedden P., et al. Genetic analysis reveals that C19-GA 2-oxidation is a major gibberellin inactivation pathway in Arabidopsis. Plant Cell. 2008;20:2420–2436. doi: 10.1105/tpc.108.058818. PubMed DOI PMC

Ueguchi-Tanaka M., Ashikari M., Nakajima M., Itoh H., Katoh E., Kobayashi M., Chow T.-Y., Hsing Y.-I.C., Kitano H., Yamaguchi I., et al. GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin. Nature. 2005;437:693–698. doi: 10.1038/nature04028. PubMed DOI

Sun T.-P. The molecular mechanism and evolution of the GA-GID1-DELLA signaling module in plants. Curr. Biol. 2011;21:R338–R345. doi: 10.1016/j.cub.2011.02.036. PubMed DOI

Hu J., Israeli A., Ori N., Sun T.-P. The Interaction between DELLA and ARF/IAA Mediates Crosstalk between Gibberellin and Auxin Signaling to Control Fruit Initiation in Tomato. Plant Cell. 2018;30:1710–1728. doi: 10.1105/tpc.18.00363. PubMed DOI PMC

De Jong M., Wolters-Arts M., Feron R., Mariani C., Vriezen W.H. The Solanum lycopersicum auxin response factor 7 (SlARF7) regulates auxin signaling during tomato fruit set and development. Plant J. 2009;57:160–170. doi: 10.1111/j.1365-313X.2008.03671.x. PubMed DOI

Goetz M., Vivian-Smith A., Johnson S.D., Koltunow A.M. AUXIN RESPONSE FACTOR8 is a negative regulator of fruit initiation in Arabidopsis. Plant Cell. 2006;18:1873–1886. doi: 10.1105/tpc.105.037192. PubMed DOI PMC

Du L., Bao C., Hu T., Zhu Q., Hu H., He Q., Mao W. SmARF8, a transcription factor involved in parthenocarpy in eggplant. Mol. Genet. Genom. 2016;291:93–105. doi: 10.1007/s00438-015-1088-5. PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...