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Transgenic cotton over-producing spinach sucrose phosphate synthase showed enhanced leaf sucrose synthesis and improved fiber quality under controlled environmental conditions

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Abstract

Prior data indicated that enhanced availability of sucrose, a major product of photosynthesis in source leaves and the carbon source for secondary wall cellulose synthesis in fiber sinks, might improve fiber quality under abiotic stress conditions. To test this hypothesis, a family of transgenic cotton plants (Gossypium hirsutum cv. Coker 312 elite) was produced that over-expressed spinach sucrose-phosphate synthase (SPS) because of its role in regulation of sucrose synthesis in photosynthetic and heterotrophic tissues. A family of 12 independent transgenic lines was characterized in terms of foreign gene insertion, expression of spinach SPS, production of spinach SPS protein, and development of enhanced extractable V max SPS activity in leaf and fiber. Lines with the highest V max SPS activity were further characterized in terms of carbon partitioning and fiber quality compared to wild-type and transgenic null controls. Leaves of transgenic SPS over-expressing lines showed higher sucrose:starch ratio and partitioning of 14C to sucrose in preference to starch. In two growth chamber experiments with cool nights, ambient CO2 concentration, and limited light below the canopy, the transgenic line with the highest SPS activity in leaf and fiber had higher fiber micronaire and maturity ratio associated with greater thickness of the cellulosic secondary wall.

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Abbreviations

AFIS:

Advanced Fiber Information System

DPA:

Days post anthesis

ELISA:

Enzyme-linked immunosorbent assay

HVI:

High-Volume Instrumentation

IFC %:

Immature fiber content expressed as a percent

KS:

Kanamycin sensitive transgenic null line

npt II:

Gene for neomycin phosphotransferase conferring kanamycin resistance

PFD:

Photon flux density

SFC %:

Short fiber content expressed as a percent

SPS:

Sucrose phosphate synthase

SPS+:

Transgenic cotton lines over-expressing spinach sucrose phosphate synthase

T0-4:

Generations of transgenic plants, with T0 being primary transformants and numbers representing further seed-propagated generations

WT:

Wild-type

References

  • Amor Y, Haigler CH, Johnson S, Wainscott M, Delmer DP (1995) A membrane-associated form of sucrose synthase and its potential role in synthesis of cellulose and callose in plants. Proc Natl Acad Sci USA 92:9353–9357

    Article  PubMed  CAS  Google Scholar 

  • Babb VM, Haigler CH (2001) Sucrose-phosphate synthase activity rises in correlation with high-rate cellulose synthesis in three heterotrophic systems. Plant Physiol 127:1234–1242

    Article  PubMed  CAS  Google Scholar 

  • Basra AS (ed) (1999) Cotton fibers: developmental biology, quality improvement, and textile processing. The Haworth Press, New York, pp 387

  • Baxter CJ, Foyer DH, Turner J, Rolfe SA, Quick WP (2003) Elevated sucrose-phosphate synthase activity in transgenic tobacco sustains photosynthesis in older leaves and alters development. J Exp Bot 54:1813–1820

    Article  PubMed  CAS  Google Scholar 

  • Bradow JM, Davidonis GW (2000) Review: quantitation of fiber quality and the cotton production-processing interface: a physiologist’s perspective. J Cotton Sci 4:34–64

    Google Scholar 

  • Chen S, Hajirezaei M, Peisker M, Tschiersch H, Sonnewald U, Börnke F (2005) Decreased sucrose-6-phosphate phosphatase level in transgenic tobacco inhibits photosynthesis, alters carbohydrate partitioning, and reduces growth. Planta 221:479–492

    Article  PubMed  CAS  Google Scholar 

  • Davidonis G, Hinojosa O (1994) Influence of seed location on cotton fiber development in planta and in vitro. Plant Sci 203:107–113

    Article  Google Scholar 

  • Foyer CH, Galtier N (1996) Source-sink interaction and communication in leaves. In: Zamski E, Schafer AA (eds) Photoassimilate distribution in plants and crops: source sink relationships. Marcel Dekker, New York, pp 311–340

    Google Scholar 

  • Galtier N, Foyer CH, Huber J, Voelker TA, Huber SC (1993) Effects of elevated sucrose-phosphate synthase activity on photosynthesis, assimilate partitioning, and growth in tomato (Lycopersicon esculentum var UC82B). Plant Physiol 101:535–543

    PubMed  CAS  Google Scholar 

  • Galtier N, Foyer CH, Murchie E, Alred R, Quick P, Voelker TA, Thépenier C, Lascève BT (1995) Effects of light and atmospheric carbon dioxide enrichment on photosynthesis and carbon partitioning in the leaves of tomato (Lycopersicon esculentum L) plants over-expressing sucrose-phosphate synthase. J Exp Bot 46:1335–1344

    CAS  Google Scholar 

  • Gipson JR (1986) Temperature effects on growth, development, and fiber properties. In: Mauney JR, Stewart JMcD (eds) Cotton physiology. The Cotton Foundation, Memphis, pp 47–56

    Google Scholar 

  • Haigler CH, Ivanova-Datcheva M, Hogan PS, Salnikov VV, Hwang S, Martin LK, Delmer DP (2001) Carbon partitioning to cellulose synthesis. Plant Mol Biol 47:29–51

    Article  PubMed  CAS  Google Scholar 

  • Haigler CH, Zhang D, Wilkerson CG (2005) Biotechnological improvement of cotton fiber maturity. Physiol Plant 124:285–294

    Article  CAS  Google Scholar 

  • Haigler CH (2007) Substrate supply for cellulose synthesis and its stress sensitivity in the cotton fiber. In: Brown RM Jr, Saxena I (eds) Cellulose molecular and structural biology. Springer, New York, pp 145–166 (in press)

  • Hendrix DL, Grange RI (1991) Carbon partitioning and export from mature cotton leaves. Plant Physiol 95:228–233

    PubMed  CAS  Google Scholar 

  • Hequet EF, Wyatt B, Abidi N, Thibodeaux DP (2006) Creation of a set of reference material for cotton fiber maturity measurements. Text Res J 76:576–586

    Article  CAS  Google Scholar 

  • Holaday AS, Chollet R (1983) Photosynthetic/photorespiratory carbon metabolism in the C3-C4 intermediate species, Moricandia arvensis and Panicum milioides. Plant Physiol 73:740–745

    PubMed  CAS  Google Scholar 

  • Hood EE, Gelvin SB, Melchers LS, Hoekema A (1993) New Agrobacterium helper plasmids for gene transfer to plants. Transgenic Res 2:208–218

    Article  CAS  Google Scholar 

  • Hsieh YL (1999) Structural development of cotton fibers and linkages to fiber quality. In: Basra AS (ed) Cotton fibers: developmental biology, quality improvement, and textile processing. The Haworth Press, New York, pp 137–166

    Google Scholar 

  • Huber SC, Huber JLA, McMichael RW (1992) The regulation of sucrose synthesis in leaves. In: Pollock CJ (ed) Carbon partitioning within and between organisms Environmental Plant Biology Series. Oxford, Bios Scientific publishers, pp 1–26

    Google Scholar 

  • Huber SC, Huber JL (1996) Role and regulation of sucrose-phosphate synthase in higher plants. Annu Rev Plant Physiol Plant Mol Biol 47:431–444

    Article  PubMed  CAS  Google Scholar 

  • Im KH (2004) Expression of sucrose-phosphate synthase (SPS) in non-photosynthetic tissues of maize. Mol Cells 17:404–409

    PubMed  CAS  Google Scholar 

  • John ME (2000) Cotton fiber-specific promoters, US Patent #6,096,950; Table 7, p 36

  • King SP (1997) Carbon and nitrogen partitioning in canola (Brassica napus L). PhD thesis, Australian National University, Australia, 114–147

  • Klein RR, Crafts-Brandner SJ, Salvucci ME (1993) Cloning and developmental expression of the sucrose-phosphate synthase gene from spinach. Planta 190:498–510

    Article  PubMed  CAS  Google Scholar 

  • Lawrence C, Holaday AS (2000) Effects of mild night chilling on respiration of expanding cotton leaves. Plant Sci 157:233–244

    Article  PubMed  CAS  Google Scholar 

  • Lunn JE, Gillespie VJ, Furbank RT (2003) Expression of a cyanobacterial sucrose-phosphate synthase from Synechocstis sp. PCC 6803 in transgenic plants. J Exp Bot 54:223–237

    Article  PubMed  CAS  Google Scholar 

  • Lunn JE, MacRae E (2003) New complexities in the synthesis of sucrose. Curr Opin Plant Biol 6:208–214

    Article  PubMed  CAS  Google Scholar 

  • Manley BFJ (ed) (1997) Randomization, bootstrap and Monte Carlo methods in Biology, 2nd edn. Chapman and Hall, London

  • Martin LK, Haigler CH (2004) Cool temperature hinders flux from glucose to sucrose during cellulose synthesis in secondary wall stage cotton fibers. Cellulose 11:339–349

    Article  CAS  Google Scholar 

  • McBride KE, Summerfelt KR (1990) Improved binary vectors for Agrobacterium-mediated plant transformation. Plant Mol Biol 14:269–276

    Article  PubMed  CAS  Google Scholar 

  • Murchie EH, Sarrobert C, Contard P, Betsche T, Foyer CH, Galtier N (1999) Over-expression of sucrose-phosphate synthase in tomato plants grown with CO2 enrichment leads to decreased foliar carbohydrate accumulation relative to untransformed controls. Plant Physiol Biochem 37:251–260

    Article  CAS  Google Scholar 

  • Ono K, Ishimaru K, Aoki N, Takahashi S, Ozawa K, Ohkawa Y, Ohsugi R (1999) Characterization of a maize sucrose-phosphate synthase protein and its effect on carbon partitioning in trnasgenic rice plants. Plant Prod Sci 2:172–177

    Article  Google Scholar 

  • Pettigrew WT (1994) Source-to-sink manipulation effects on cotton fiber quality. Agron J 87:947–952

    Article  Google Scholar 

  • Pierce FT, Lord E (1939) The fineness and maturity of cotton. J Text Inst 30:T173–T210

    Google Scholar 

  • Restrep MA, Freed DD, Carrington JC (1990) Nuclear transport of plant potyviral proteins. Plant Cell 2:987–998

    Article  Google Scholar 

  • Roberts EM, Nunna RR, Huang JY, Trolinder NL, Haigler CH (1992) Effects of cycling temperatures on fiber metabolism in cultured cotton ovules. Plant Physiol 100:979–986

    PubMed  CAS  Google Scholar 

  • Sambrook J, Russel DW (2001) Molecular cloning, a laboratory manual 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York

    Google Scholar 

  • Schubert AM, Benedict CR, Kohel RJ (1986) Carbohydrate distribution in bolls. In: Mauney JR, Stewart McDJ (eds) Cotton physiology, Cotton Foundation, Memphis, pp 311–324

    Google Scholar 

  • Signora L, Galtier N, SkØt L, Hélène L, Foyer CH (1998) Over-expression of sucrose-phosphate synthase in Arabidopsis thaliana results in increased foliar sucrose/starch ratios and favours decreased foliar carbohydrate accumulation in plants after prolonged growth with CO2 enrichment. J Exp Bot 49:669–680

    Article  CAS  Google Scholar 

  • Singh B, Haley L, Nightengale J, Kang WH, Haigler CH, Holaday AS (2005) Long-term night chilling of cotton, Gossypium hirsutum, does not result in reduced CO2 assimilation. Func Plant Biol 32:655–666

    Article  Google Scholar 

  • Stitt M (1989) Control analysis of photosynthetic sucrose synthesis: assignment of elasticity coefficients and flux-control coefficients to the cytosolic fructose 1,6-bisphosphatase and sucrose-phosphate synthase. Phil Trans R Soc Lond B 323:327–338

    CAS  Google Scholar 

  • Stitt M (1990) Fructose-2,6-bisphosphate as a regulatory molecule in plants. Annu Rev Plant Physiol Plant Mol Biol 41:153–185

    Article  CAS  Google Scholar 

  • Tarczynski MC, Byrne DN, Miller WB (1992) High performance liquid chromatography analysis of carbohydrates of cotton-phloem sap and of honeydew produced by Bemisia tabaci feeding on cotton. Plant Physiol 98:753–756

    Article  PubMed  CAS  Google Scholar 

  • Toroser D, Athwal GS, Huber SC (1998) Site-specific regulatory interaction between spinach leaf sucrose-phosphate synthase and 14-3-3 proteins. FEBS Lett 435:110–114

    Article  PubMed  CAS  Google Scholar 

  • Toroser D, McMichael R Jr, Krause KP, Kurreck J, Sonnewald U, Stitt M, Huber SC (1999) Site-directed mutagenesis of serine 158 demonstrates its role in spinach leaf sucrose-phosphate synthase modulation. Plant J 17:407–413

    Article  PubMed  CAS  Google Scholar 

  • Tummala J (1996) Response of sucrose-phosphate synthase activity to cool temperatures in cotton. MS thesis, Texas Tech University, Lubbock, TX, USA

  • Umbeck P, Swain W, Yang NS (1989) Inheritance and expression of genes for kanamycin and chloramphenicol resistance in transgenic cotton plants. Crop Sci 29:196–201

    Article  CAS  Google Scholar 

  • Updegraff DM (1969) Semi-micro determination of cellulose in biological materials. Anal Biochem 32:420–424

    Article  PubMed  CAS  Google Scholar 

  • Walker JL, Huber SC (1989) Puification and preliminary characterization of sucrose-phosphate synthase using monoclonal antibodies. Plant Physiol 89:518–524

    PubMed  CAS  Google Scholar 

  • Warner DA, Holaday AS, Burke JJ (1995) Response of carbon metabolism to night temperatures in cotton. Agron J 87:1193–1197

    Article  Google Scholar 

  • Wilkins TA, Wan CY, Lu CC (1994) Ancient origin of the vacuolar H+-ATPase 69-kilodalton catalytic subunit superfamily. Theor Appl Genet 89:514–524

    Article  CAS  Google Scholar 

  • Wilkins TA, Smart LB (1996) Isolation of RNA from plant tissue. In: Krieg A (ed) Laboratory guide to RNA: isolation, analysis, and synthesis, Wiley Liss, New York, pp 21–40

    Google Scholar 

  • Winter H, Huber SC (2000) Regulation of sucrose metabolism in higher plants: Localization and regulation of activity of key enzymes. Crit Rev Plant Sci 19:31–67

    Article  CAS  Google Scholar 

  • Worrell AC, Bruneau JM, Summerfelt K, Boersig M, Voelker T (1991) Expression of maize sucrose-phosphate synthase in tomato alters carbohydrate partitioning. Plant Cell 3:1121–1130

    Article  PubMed  CAS  Google Scholar 

  • Xu B, Huang Y (2004) Image Analysis for Cotton Fibers, Part II: Cross-Sectional Measurement. Textile Res J 74:409–416

    CAS  Google Scholar 

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Acknowledgments

Two anonymous reviewers are thanked for helpful comments. For providing materials, we thank Drs. Steve Huber (antibody to spinach SPS), Norma Trolinder (seeds of elite highly regenerable selections of G.h. cv Coker 312), and Hong Zhang (fragment of Arabidopsis 18S ribosomal RNA gene). For technical advice or assistance we thank: Norma Trolinder (training in cotton regeneration), Cory Reed and Michelle Morales (assistance with statistical analyses), Robert Wright (suggestions on DNA blotting protocol), and Tahan Jaradat, Nagurar Srinivas, and Melody Wainscott (preliminary analysis of SPS+ plant lines). FIAS software was developed by Dr. B. Xu (Univ. Texas-Austin). For funding and/or in-kind support of this work, we thank Cotton Incorporated Cary NC, the Texas Advanced Research, Technology, and Technology Development and Transfer Programs, the Phytotron of Duke University, the Texas Food and Fiber Commission, and Bayer CropScience.

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Correspondence to Candace H. Haigler.

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Haigler, C.H., Singh, B., Zhang, D. et al. Transgenic cotton over-producing spinach sucrose phosphate synthase showed enhanced leaf sucrose synthesis and improved fiber quality under controlled environmental conditions. Plant Mol Biol 63, 815–832 (2007). https://doi.org/10.1007/s11103-006-9127-6

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