Abstract
Key message
Sink-specific expression of a sucrose transporter protein gene from the C4 plant maize can promote carbohydrate accumulation in target tissues and increase both fiber and seed yield of cotton.
Abstract
Sucrose is the principal form of photosynthetic products transported from source tissue to sink tissue in higher plants. Enhancing the partition of carbohydrate to the target organ is a promising way to improve crop productivity. The C4 plant Zea mays exhibits a substantially higher rate of export of photosynthates than many C3 plants, and its sucrose transporter protein ZmSut1 displays important role in sucrose allocation. To investigate how use of ZmSUT1 gene to increase the fiber and seed yield of cotton, in this study, we expressed the gene in cotton under a senescence-inducible promoter PSAG12 and a seed coat-specific promoter BAN, respectively. We show that senescence-induced expression of ZmSUT1 results in an increase of sugar accumulation in leaves. Although the leaf senescence was postponed in PSAG12::ZmSUT1 cotton, the photosynthetic rate of the leaves was decreased. In contrast, seed coat-specific expression of the gene leads to an increase of sugar accumulation in fibers and bolls, and the leaf of transgenic BAN::ZmSUT1 cotton displayed higher photosynthetic capacity than the wild type. Importantly, both fiber and seed yield of transgenic BAN::ZmSUT1 cotton are significantly enhanced. Our data indicate the potential of enhancing yield of carbohydrate crops by the regulation of sugar partitioning.
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References
Ainsworth EA, Bush DR (2011) Carbohydrate export from the leaf: a highly regulated process and target to enhance photosynthesis and productivity. Plant Physiol 155:64–69. https://doi.org/10.1104/pp.110.167684
Aoki N (1999) Molecular cloning and expression analysis of a gene for a sucrose transporter in maize (Zea mays L.). Plant Cell Physiol 40:1072–1078
Ayre BG (2011) Membrane-transport systems for sucrose in relation to whole-plant carbon partitioning. Mol Plant 4:377–394. https://doi.org/10.1093/mp/ssr014
Baker RF, Leach KA, Boyer NR, Swyers MJ, Benitez-Alfonso Y, Skopelitis T, Luo A, Sylvester A, Jackson D, Braun DM (2016) Sucrose transporter ZmSut1 expression and localization uncover new insights into sucrose phloem loading. Plant Physiol 172:1876–1898. https://doi.org/10.1104/pp.16.00884
Bihmidine S, Hunter CT 3rd, Johns CE, Koch KE, Braun DM (2013) Regulation of assimilate import into sink organs: update on molecular drivers of sink strength. Front Plant Sci 4:177. https://doi.org/10.3389/fpls.2013.00177
Carpaneto A, Geiger D, Bamberg E, Sauer N, Fromm J, Hedrich R (2005) Phloem-localized, proton-coupled sucrose carrier ZmSUT1 mediates sucrose efflux under the control of the sucrose gradient and the proton motive force. J Biol Chem 280:21437. https://doi.org/10.1074/jbc.M501785200
Chincinska IA, Liesche J, Krügel U, Michalska J, Geigenberger P, Grimm B, Kühn C (2008) Sucrose transporter StSUT4 from potato affects flowering, tuberization, and shade avoidance response. Plant Physiol 146:515–528. https://doi.org/10.1104/pp.107.112334
Chory J, Reinecke D, Sim S, Washburn T, Brenner M (1994) A role for cytokinins in de-etiolation in Arabidopsis (det mutants have an altered response to cytokinins). Plant Physiol 104:339–347
Debeaujon I, Nesi N, Perez P, Devic M, Grandjean O, Caboche M, Lepiniec L (2003) Proanthocyanidin-accumulating cells in Arabidopsis testa: regulation of differentiation and role in seed development. Plant Cell 15:2514–2531. https://doi.org/10.1105/tpc.014043
Dhindsa RS, Plumb-Dhindsa P, Thorpe TA (1981) Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. J Exp Bot 32:93–101
Grbić V, Bleecker AB (1995) Ethylene regulates the timing of leaf senescence in Arabidopsis. Plant J 8:595–602
Griffiths CA, Paul MJ (2017) Targeting carbon for crop yield and drought resilience. J Sci Food Agr. https://doi.org/10.1002/jsfa.8501
Grodzinski B, Jiao J, Leonardos ED (1998) Estimating photosynthesis and concurrent export rates in C3 and C4 species at ambient and elevated CO2. Plant Physiol 117:207–215. https://doi.org/10.1104/pp.117.1.207
Hall AJ, Brady CJ, Hall AJ, Brady CJ (1977) Assimilate source-sink relationships in Capsicum annuum L. II. Effects of fruiting and defloration on the photosynthetic capacity and senescence of the leaves. Funct Plant Biol 4:771–783
Hc JVR, Van den Ende W (2018) UDP-glucose: a potential signaling molecule in plants? Front Plant Sci 8:2230. https://doi.org/10.3389/fpls.2017.02230
Hodgkinson K (1974) Influence of partial defoliation on photosynthesis, photorespiration and transpiration by lucerne leaves of different ages. Funct Plant Biol 1:561–578. https://doi.org/10.1071/PP9740561
Iglesias DJ, Lliso I, Tadeo FR, Talon M (2002) Regulation of photosynthesis through source: sink imbalance in citrus is mediated by carbohydrate content in leaves. Physiol Plantarum 116:563–572. https://doi.org/10.1034/j.1399-3054.2002.1160416.x
Jeffrey ZC, Scheffler BE, Elizabeth D, Triplett BA, Tianzhen Z, Wangzhen G, **aoya C, Stelly DM, Rabinowicz PD, Town CD (2007) Toward sequencing cotton (Gossypium) genomes. Plant Physiol 145:1303–1310. https://doi.org/10.1104/pp.107.107672
Jiang Y, Guo W, Zhu H, Ruan YL, Zhang T (2012) Overexpression of GhSusA1 increases plant biomass and improves cotton fiber yield and quality. Plant Biotechnol J 10:301–312. https://doi.org/10.1111/j.1467-7652.2011.00662.x
Kaschuk G, Hungria M, Leffelaar PA, Giller KE, Kuyper TW (2010) Differences in photosynthetic behaviour and leaf senescence of soybean (Glycine max [L.] Merrill) dependent on N2 fixation or nitrate supply. Plant Biol 12:60–69
Kong X, Luo Z, Dong H, Eneji AE, Li W, Lu H (2013) Gene expression profiles deciphering leaf senescence variation between early- and late-senescence cotton lines. PLoS One 8:e69847. https://doi.org/10.1371/journal.pone.0069847
Kusaba M, Ito H, Morita R, Iida S, Sato Y, Fujimoto M, Kawasaki S, Tanaka R, Hirochika H, Nishimura M (2007) Rice NON-YELLOW COLORING1 is involved in light-harvesting complex II and grana degradation during leaf senescence. Plant Cell 19:1362–1375. https://doi.org/10.1105/tpc.106.042911
Li L, Sheen J (2016) Dynamic and diverse sugar signaling. Curr Opin Plant Biol 33:116–125. https://doi.org/10.1016/j.pbi.2016.06.018
Luo M, **ao Y, Li X, Lu X, Deng W, Li D, Hou L, Hu M, Li Y, Pei Y (2010) GhDET2, a steroid 5α-reductase, plays an important role in cotton fiber cell initiation and elongation. Plant J 51:419–430. https://doi.org/10.1111/j.1365-313X.2007.03144.x
Marschall M, Proctor MCF, Smirnoff N (1998) Carbohydrate composition and invertase activity of the leafy liverwort Porella platyphylla. New Phytol 138:343–353. https://doi.org/10.1046/j.1469-8137.1998.00102.x
McCormick AJ, Cramer MD, Watt DA (2006) Sink strength regulates photosynthesis in sugarcane. New Phytol 171:759–770. https://doi.org/10.1111/j.1469-8137.2006.01785.x
Meredith WR, Wells R (1989) Potential for increasing cotton yields through enhanced partitioning to reproductive structures. Crop Sci 29:636–639. https://doi.org/10.2135/cropsci1989.0011183X002900030017x
Miller PA, Rawlings JO (1967) Selection for increased lint yield and correlated responses in upland cotton, Gossypium hirsutum L. Crop Sci 7:637–640. https://doi.org/10.2135/cropsci1967.0011183X000700060024x
Miller DA, Williams JC, Robinson HF, Comstock JB (1958) Estimates of genotypic and environmental variances and co variances in upland cotton and their implication in selection. Agron J 50:126–131. https://doi.org/10.2134/agronj1958.00021962005000030004x
Noh YS, Amasino RM (1999) Identification of a promoter region responsible for the senescence-specific expression of SAG12. Plant Mol Biol 41:181–194
Ori N, Juarez MT, Jackson D, Yamaguchi J, Banowetz GM, Hake S (1999) Leaf senescence is delayed in tobacco plants expressing the maize homeobox gene knotted1 under the control of a senescence-activated promoter. Plant Cell 11:1073–1080. https://doi.org/10.1105/tpc.11.6.1073
Otegui MS, Noh YS, Martinez DE, Vila Petroff MG, Staehelin LA, Amasino RM, Guiamet JJ (2005) Senescence-associated vacuoles with intense proteolytic activity develop in leaves of Arabidopsis and soybean. Plant J 41:831–844. https://doi.org/10.1111/j.1365-313X.2005.02346.x
Paul MJ, Foyer CH (2001) Sink regulation of photosynthesis. J Exp Bot 52:1383–1400. https://doi.org/10.1093/jexbot/52.360.1383
Paul MJ, Pellny TK (2003) Carbon metabolite feedback regulation of leaf photosynthesis and development. J Exp Bot 54:539–547. https://doi.org/10.1093/jxb/erg052
Riesmeier JW, Willmitzer L, Frommer WB (1992) Isolation and characterization of a sucrose carrier cDNA from spinach by functional expression in yeast. EMBO J 11:4705. https://doi.org/10.1002/j.1460-2075.1992.tb05575.x
Rook F, Bevan MW (2003) Genetic approaches to understanding sugar-response pathways. J Exp Bot. https://doi.org/10.1093/jxb/erg054
Ruan YL (2005) Recent advances in understanding cotton fibre and seed development Seed. Sci Res 15:269–280. https://doi.org/10.1079/ssr2005217
Sauer N (2007) Molecular physiology of higher plant sucrose transporters. FEBS Lett 581:2309–2317. https://doi.org/10.1016/j.febslet.2007.03.048
Sheen J (1990) Metabolic repression of transcription in higher plants. Plant Cell 2:1027. https://doi.org/10.1105/tpc.2.10.1027
Slewinski TL, Garg A, Johal GS, Braun DM (2010) Maize SUT1 functions in phloem loading. Plant Signal Behavior 5:687–690. https://doi.org/10.4161/psb.5.6.11575
Smeekens S (2000) Sugar-induced signal transduction in plants. Annu Rev Plant Mol Bio 51:49–81. https://doi.org/10.1146/annurev.arplant.51.1.49
Stitt M, Lunn J, Usadel B (2010) Arabidopsis and primary photosynthetic metabolism—more than the icing on the cake. Plant J 61:1067–1091. https://doi.org/10.1111/j.1365-313X.2010.04142.x
Thimann KV, Tetley RM, Krivak BM (1977) Metabolism of oat leaves during senescence: V. senescence in light. Plant Physiol 59:448–454. https://doi.org/10.1104/pp.65.5.855
Usha B, Bordoloi D, Parida A (2015) Diverse expression of sucrose transporter gene family in Zea mays. J Genet 94:151–154. https://doi.org/10.1007/s12041-015-0491-3
Wang L, Lu Q, Wen X, Lu C (2015) Enhanced sucrose loading improves rice yield by increasing grain size. Plant Physiol 169:2848–2862. https://doi.org/10.1104/pp.15.01170
Weichert N, Saalbach I, Weichert H, Kohl S, Erban A, Kopka J, Hause B, Varshney A, Sreenivasulu N, Strickert M, Kumlehn J, Weschke W, Weber H (2010) Increasing sucrose uptake capacity of wheat grains stimulates storage protein synthesis. Plant Physiol 152:698–710. https://doi.org/10.1104/pp.109.150854
Xu SM, Brill E, Llewellyn DJ, Furbank RT, Ruan YL (2012) Overexpression of a potato sucrose synthase gene in cotton accelerates leaf expansion, reduces seed abortion, and enhances fiber production. Mol Plant 5:430–441. https://doi.org/10.1093/mp/ssr090
Zeng LH, Meredith WR, Boykin DL, Taliercio E (2007) Evaluation of an exotic germplasm population derived from multiple crosses among Gossypium tetraploid species. J Cotton Sci 11:118–127
Zhang M, Zheng X, Song S, Zeng Q, Hou L, Li D, Zhao J, Wei Y, Li X, Luo M (2011) Spatiotemporal manipulation of auxin biosynthesis in cotton ovule epidermal cells enhances fiber yield and quality. Nat Biotechnol 29:453–458. https://doi.org/10.1038/nbt.1843
Zhang M, Zeng J, Long H, **ao Y, Yan X, Pei Y (2017) Auxin regulates cotton fiber initiation via GhPIN-mediated auxin transport. Plant Cell Physiol 58:385–397. https://doi.org/10.1093/pcp/pcw203
Zhao DL, Mackown CT, Starks PJ, Kindiger BK (2010) Rapid analysis of nonstructural carbohydrate components in grass forage using microplate enzymatic assays. Crop Sci 50:1537–1545. https://doi.org/10.2135/cropsci2009.09.0521
Zhao J, Bai W, Zeng Q, Song S, Mi Z, Li X, Lei H, **ao Y, Ming L, Li D (2015) Moderately enhancing cytokinin level by down-regulation of GhCKX expression in cotton concurrently increases fiber and seed yield. Mol Breed 35:60. https://doi.org/10.1007/s11032-015-0232-6
Acknowledgements
This study was funded by National Major Project of Breeding of China (2016YFD0100505 to YP and 2018YFD0100403 to XL), National Transgenic New Species Breeding Major Project of China (2016ZX08005-003-004 to YP) and Natural Science Foundation of China (31130039 to YP).
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Ding, X., Zeng, J., Huang, L. et al. Senescence-induced expression of ZmSUT1 in cotton delays leaf senescence while the seed coat-specific expression increases yield. Plant Cell Rep 38, 991–1000 (2019). https://doi.org/10.1007/s00299-019-02421-1
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DOI: https://doi.org/10.1007/s00299-019-02421-1