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Plant function and evolutionary biology
RESEARCH ARTICLE

Expression of sucrose synthase in the developing endosperm is essential for early seed development in cotton

Yong-Ling Ruan A D , Danny J. Llewellyn B , Qing Liu B , Shou-Min Xu B , Li-Min Wu B , Lu Wang C and Robert T. Furbank B
+ Author Affiliations
- Author Affiliations

A School of Environmental and Life Sciences, The University of Newcastle, Callaghan, NSW 2308, Australia.

B CSIRO Plant Industry, GPO Box 1600, Canberra, ACT 2601, Australia.

C Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai 200032, China.

D Corresponding author. Email: yong-ling.ruan@newcastle.edu.au

Functional Plant Biology 35(5) 382-393 https://doi.org/10.1071/FP08017
Submitted: 25 January 2008  Accepted: 1 May 2008   Published: 11 July 2008

Abstract

Successful seed development requires coordinated interaction of the endosperm and embryo. In most dicotyledonous seeds, the endosperm is crushed and absorbed by the expanding embryo in the later stages of seed development. Little is known about the metabolic interaction between the two filial tissues early in seed development. We examined the potential role of sucrose synthase (Sus) in the endosperm development of cotton. Sus was immunologically localised in the cellularising endosperm, but not in the heart-stage embryo at 10 days after anthesis. The activities of Sus and acid invertase were significantly higher in the endosperm than in the young embryos, which corresponded to a steep concentration difference in hexoses between the endosperm and the embryo. This observation indicates a role for the endosperm in generating hexoses for the development of the two filial tissues. Interestingly, Sus expression and starch deposition were spatially separated in the seeds. Silencing the expression of Sus in the endosperm using an RNAi approach led to the arrest of early seed development. Histochemical analyses revealed a significant reduction in cellulose and callose in the deformed endosperm cells of the Sus-suppressed seed. The data indicate a critical role of Sus in early seed development through regulation of endosperm formation.

Additional keywords: embryo, gene silencing, Sus.


Acknowledgements

We thank Dr Mark Talbot for excellent technical assistance in the fluorescent labelling of cellulose. We are grateful to Joanne Page for conducting cotton transformation.


References


Amor Y, Haigler CH, Johnson S, Wainscott M, Delmer DP (1995) A membrane-associated form of Sus and its potential role in synthesis of cellulose and callose in plants. Proceedings of the National Academy of Sciences of the United States of America 92, 9353–9357.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Bate N, Niu X, Wang Y, Reimann KS, Helentjaris TG (2004) An invertase inhibitor from maize localizes to the embryo surrounding region during early kernel development. Plant Physiology 134, 246–254.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Baud S, Wuilleme S, Lemoine R, Kronenberger J, Caboche M, Lepiniec L, Rochat C (2005) The AtSUC5 sucrose transporter specifically expressed in the endosperm is involved in early seed development in Arabidopsis. The Plant Journal 43, 824–836.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Berger F (1999) Endosperm development. Current Opinion in Plant Biology 2, 28–32.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Bieniawska Z, Barratt DHP, Garlick AP, Thole V, Kruger NJ, Martin C, Zrenner R, Smith AM (2007) Analysis of the sucrose synthase gene family in Arabidopsis. The Plant Journal 49, 810–828.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Blanton RL (1993) Prestalk cells in monolayer cultures exhibit two distinct modes of cellulose synthesis during stalk cell differentiation in Dictyostelium. Development 119, 703–710. open url image1

Borisjuk L, Walenta S, Rolletschek H, Mueller-Klieser W, Wobus U, Weber H (2002) Spatial analysis of plant metabolism: sucrose imaging within Vicia faba cotyledons reveals specific developmental patterns. The Plant Journal 29, 521–530.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Carlson SJ, Chourey PS (1996) Evidence for plasma membrane-associated forms of sucrose synthase in maize. Molecular & General Genetics 252, 303–310. open url image1

Chaudhury AM, Ming L, Miller C, Craig S, Dennis ES, Peacock WJ (1997) Fertilization-independent seed development in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America 94, 4223–4228.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Chaudhury AM, Koltunow A, Payne T, Ming L, Tucker MR, Dennis ES, Peacock WJ (2001) Control of early seed development. Annual Review of Cell and Developmental Biology 17, 677–699.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Cheng W-H, Taliercio EW, Chourey PS (1996) The Miniature seed locus of maize encodes a cell-wall invertase required for normal development of endosperm and maternal cells in the pedicel. The Plant Cell 8, 971–983.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Chourey PS, Taliercio EW, Carlson SJ, Ruan Y-L (1998) Genetic evidence that the two isozymes of sucrose synthase present in developing maize endosperm are critical, one for cell wall integrity and the other for starch biosynthesis. Molecular & General Genetics 259, 88–96.
Crossref | GoogleScholarGoogle Scholar | open url image1

Doblin MS, Kurek I, Jacon-Wilk D, Delmer DP (2002) Cellulose biosynthesis in plants: from genes to rosettes. Plant & Cell Physiology 43, 1407–1420.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Haigler CH, Ivanova-Datcheva M, Hogan PS, Salnikov VV, Hwang S, Martin K, Delmer DP (2001) Carbon partitioning to cellulose synthesis. Plant Molecular Biology 47, 29–51.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hill LM, Morley-Smith ER, Rawsthorne S (2003) Metabolism of sugars in the endosperm of developing seeds of oilseed Rape. Plant Physiology 131, 228–236.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hirner B, Fischer WN, Rentsch D, Kwart M, Frommer WB (1998) Developmental control of H+/amino acid permease gene expression during seed development of Arabidopsis. The Plant Journal 14, 535–544.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hirose T, Takano M, Terao T (2002) Cell wall invertase in developing rice caryopsis: Molecular cloning of OsCIN1 and analysis of its expression in relation to its role in grain filling. Plant & Cell Physiology 43, 452–459.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusion: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. The EMBO Journal 6, 3901–3907.
PubMed |
open url image1

King SP, Lunn JE, Furbank RT (1997) Carbohydrate content and enzyme metabolism in developing canola siliques. Plant Physiology 114, 153–160.
PubMed |
open url image1

Koch K (2004) Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Current Opinion in Plant Biology 7, 235–246.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Liu Q, Singh SP, Brubaker CL, Sharp PJ, Green AG, Marshall DR (1999) Molecular cloning and expression of a cDNA encoding a microsomal ω-6 fatty acid desaturase from cotton (Gossypium hirsutum). Australian Journal of Plant Physiology 26, 101–106. open url image1

Meikle PJ, Bonig I, Hoogenraad NJ, Clarke AE, Stone BA (1991) The location of (1→3)-β-glucans in the walls of pollen tubes of Nicotiana alata using a (1→3)-β-glucan-specific monoclonal antibody. Planta 185, 1–8.
Crossref | GoogleScholarGoogle Scholar | open url image1

Patrick JP, Offler CE (1995) Post-sieve element transport of sucrose in developing seeds. Australian Journal of Plant Physiology 22, 681–702. open url image1

Ruan Y-L (2005) Recent advances in understanding cotton fibre and seed development. Seed Science Research 15, 269–280.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ruan Y-L (2007) Rapid cell expansion and cellulose synthesis regulated by plasmodesmata and sugar: insights from the single-celled cotton fibre. Functional Plant Biology 34, 1–10.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ruan Y-L, Chourey PS (1998) A fibreless seed mutation in cotton is associated with lack of fibre cell initiation in ovule epidermis and alterations in sucrose synthase expression and carbon partitioning in developing seeds. Plant Physiology 118, 399–406.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ruan Y-L , Chourey PS (2006). Carbon partitioning in developing seed. In ‘Seed sciences and technology: trends and advances’. (Ed. AS Basra) pp. 125–152. (The Haworth Press: New York.)

Ruan Y-L, Chourey PS, Delmer PD, Perez-Grau L (1997) The differential expression of sucrose synthase in relation to diverse patterns of carbon partitioning in developing cotton seed. Plant Physiology 115, 375–385.
PubMed |
open url image1

Ruan Y-L, Llewellyn DJ, Furbank RT (2001) The control of single-celled cotton fibre elongation by developmentally reversible gating of plasmodesmata and coordinated expression of sucrose and K+ transporters and expansin. The Plant Cell 13, 47–63.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ruan Y-L, Llewellyn DJ, Furbank RT (2003) Suppression of sucrose synthase expression represses cotton fibre cell initiation, elongation and seed development. The Plant Cell 15, 952–964.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ruan Y-L, Xu S-M, White R, Furbank RT (2004) Genotypic and developmental evidence for the role of plasmodesmatal regulation in cotton fibre elongation mediated by callose turnover. Plant Physiology 136, 4104–4113.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Salnikov VV, Grimson MJ, Delmer DP, Haigler CH (2001) Sucrose synthase localizes to cellulose synthesis sites in tracheary elements. Phytochemistry 57, 823–833.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Salnikov VV, Grimson MJ, Seagull RW, Haigler CH (2003) Localization of sucrose synthase and callose in freeze-substituted secondary wall-stage cotton fibres. Protoplasma 221, 175–184.
PubMed |
open url image1

Schünmann PHD, Llewellyn D, Surin B, Boevink P, Defeyter RC, Waterhouse PM (2003) A suite of novel promoters and terminators for plant biotechnology. Functional Plant Biology 30, 443–452.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sørensen MB, Mayer U, Lukowitz W, Robert H, Chambrier P, Jurgens G, Somerville C, Lepiniec L, Berger F (2002) Cellularisation in the endosperm of Arabidopsis thaliana is coupled to mitosis and shares multiple components with cytokinesis. Development 129, 5567–5576.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Stewart JM (1986). Integrated events in the flower and fruit. In ‘Cotton physiology’. (Eds JR Mauney, JM Stewart) pp. 261–300. (Cotton Foundation: Memphis.)

Tomlinson KL, McHugh S, Labbe H, Grainger JL, James LE, Pomeroy KM, Mullin JW, Miller SS, Dennis DT, Miki BLA (2004) Evidence that the hexose-to-sucrose ratio does not control the switch to storage product accumulation in oilseeds: analysis of tobacco seed development and effects of overexpressing apoplastic invertase. Journal of Experimental Botany 55, 2291–2303.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Waterhouse PM, Wang MB, Finnegan EJ (2001) Role of the short RNAs in gene silencing. Trends in Plant Science 6, 297–301.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Weber H, Borisjuk L, Heim U, Buchner P, Wobus U (1995) Seed coat-associated invertase of faba bean control both unloading and storage functions: cloning of cDNAs and cell type-specific expression. The Plant Cell 7, 1835–1846.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Weber H, Buchner P, Borisjuk L, Wobus U (1996) Sucrose metabolism during cotyledon development of Vicia faba L. is controlled by the concerted action of both sucrose-phosphate synthase and sucrose synthase: expression patterns, metabolic regulation and implications for seed development. The Plant Journal 9, 841–850.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Weber H, Borisjuk L, Heim U, Wobus U (1997) Sugar import and metabolism during seed development. Trends in Plant Science 2, 169–174.
Crossref | GoogleScholarGoogle Scholar | open url image1

Weber H, Borisjuk L, Wobus U (2005) Molecular physiology of legume seed development. Annual Review of Plant Biology 56, 253–279.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Zhang W-H, Zhou Y, Dibley KE, Tyerman SD, Furbank RT, Patrick JW (2007) Nutrient loading of developing seeds. Functional Plant Biology 34, 314–331.
Crossref | GoogleScholarGoogle Scholar | open url image1

Zrenner R, Salanoubat M, Willmitzer L, Sonnewald U (1995) Evidence of the crucial role of sucrose synthase for sink strength using transgenic potato plants (Solanum tuberosum L.). The Plant Journal 7, 97–107.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1