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Journal of Integrative Agriculture  2013, Vol. 12 Issue (3): 406-413    DOI: 10.1016/S2095-3119(13)60240-3
Crop Genetics · Breeding · Germplasm Resources Advanced Online Publication | Current Issue | Archive | Adv Search |
Relationships Between C4 Enzyme Activities and Yield in Soybeans (Glycine max (L.) Merr.)
 HUANG Shan-shan, LI Chang-suo, YANG Ming-liang, LI Wen-bin , WANG Ji-an
1.Key Laboratory of Soybean Biology, Ministry of Education/Soybean Research Institute, Northeast Agricultural University, Harbin 150030, P.R.China
2.Plant Protection Institute, Heilongjiang Academy of Land Reclamation Sciences, Harbin 150038, P.R.China
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摘要  To study the relationships between C4 enzyme activities and yield, C4 enzyme activities (phosphoenolpyruvate carboxylase (PEPCase), NADP-malate dehydrogenase (NADP-MDH), NADP-malic enzyme (NADP-ME), and pyruvate phosphate dikinase (PPDK)) in different organs of ten soybean cultivars with different yields were measured at different growth stages in China. The result showed that four enzyme activities in C4 pathway were obviously different among cultivars, especially PPDK activity was not detected in the leaves of Dongnong 1567 and Dongnong 1068 and the young leaves of Gongjiao 9107-1 and Dongnong 97-172, but there were weak activities in pod coats. The order of C4 enzyme activities is young leaves < old leaves < pod coats. The correlation coefficients between PEPCase activity and yield and between NADP-MDH activity at blooming stage and yield were 0.6979 and 0.6565, respectively, and both reached the significant level (5%), and PEPCase activity kept significant positive correlation with plant photosynthetic rate. There was a negative correlation between NADP-ME activity and yield, and no correlation was found between PPDK activity and yield.

Abstract  To study the relationships between C4 enzyme activities and yield, C4 enzyme activities (phosphoenolpyruvate carboxylase (PEPCase), NADP-malate dehydrogenase (NADP-MDH), NADP-malic enzyme (NADP-ME), and pyruvate phosphate dikinase (PPDK)) in different organs of ten soybean cultivars with different yields were measured at different growth stages in China. The result showed that four enzyme activities in C4 pathway were obviously different among cultivars, especially PPDK activity was not detected in the leaves of Dongnong 1567 and Dongnong 1068 and the young leaves of Gongjiao 9107-1 and Dongnong 97-172, but there were weak activities in pod coats. The order of C4 enzyme activities is young leaves < old leaves < pod coats. The correlation coefficients between PEPCase activity and yield and between NADP-MDH activity at blooming stage and yield were 0.6979 and 0.6565, respectively, and both reached the significant level (5%), and PEPCase activity kept significant positive correlation with plant photosynthetic rate. There was a negative correlation between NADP-ME activity and yield, and no correlation was found between PPDK activity and yield.
Keywords:  soybean       photosynthetic rate       yield       C4 enzyme  
Accepted:
Fund: 

This study was supported by the National Natural Science Foundation of China (30471092) and the Genetically Modified Organisms Breeding Major Projects, China (2009ZX08009- 089B).

Corresponding Authors:  Correspondence WANG Ji-an, Tel: +86-451-55190692, E-mail: wangsoy@yahoo.com.cn      E-mail:  wangsoy@yahoo.com.cn
About author:  HUANG Shan-shan, E-mail: huangshanshan.6@163.com

Cite this article: 

HUANG Shan-shan, LI Chang-suo, YANG Ming-liang, LI Wen-bin , WANG Ji-an. 2013. Relationships Between C4 Enzyme Activities and Yield in Soybeans (Glycine max (L.) Merr.). Journal of Integrative Agriculture, 12(3): 406-413.

[1]Aoyagi K, Chua N H. 1988. Cell-specific expression ofpyruvate, Pidikinase in situ mRNA hybridization andimmunolocalization labeling of protein in wheat seed.Plant Physiology, 86, 364-368

[2]Blanke M M, Lenz F. 1989. Fruit photosynthesis. PlantCell and Environment, 12, 31-46

[3]Brown N J, Parsley K, Hibberd J M. 2005. The future of C4research-maize, flaveria or cleome trends. Plant Science,10, 215-221

[4]Cerling T E, Harris J M, Macfadden B J, Leasey M G, QuadeJ, Eisenmann V, Ehleringer J R. 1997. Global vegetationchange through the Miocene/Pliocene boundary.Nature, 389, 153-158

[5]Chinthapalli B, Murmu J, Raghavendra A S. 2003. Dramaticdifference in the responses of phosphoenolpyruvatecarboxylase to temperature in leaves of C3 and C4 plants.Journal of Experimental Botany, 54, 707-714

[6]Chollet R, Vidal J, O’Leary M H. 1996. Phosphoenolpyruvatecarboxylase: a ubiquitous, highly regulated enzyme inplants. Annual Review of Plant Physiology PlantMolecular Biology, 47, 273-298

[7]Duffus C M, Rosie R. 1973. Some enzyme activitiesassociated with the chlorophyll containing layers ofimmature barley pericarp. Planta, 114, 219-226

[8]Edwards G E, Ku M S B, Hatch M D. 1982. Photosynthesis inPanicum milioides, a species with reduced photorespiration.Plant and Cell Physiology, 23, 1185-1195

[9]Edwards G E, Walker D. 1983. Comparative studies of C3,C4 metabolism in other plant tissue. In: Edwards G E,Walker D, eds., C3, C4: Mechanisms, and Cellular andEnvironmental Regulation, of Photosynthesis. BlackwellScientific Publications, England. pp. 479-495

[10]Gayathri J, Parvathi K, Raghavendra A S. 2000. Purificationand stability during storage of phosphoenolpyruvatecarboxylase from leaves of Amaranthus hypochondriacus,a NAD-ME type C4 plant. Photosynthetica, 38, 45-52

[11]Gehlen J, Panstruga R, Smets H, Merkelbach S, Kleines M,Porsch P, Fladung M, Becker I, Rademacher T, HauslerR E, et al. 1996. Effects of altered phosphoenolpyruvatecarboxylase activities on transgenic C3 plant Solanumtuberosum. Plant Molecular Biology, 32, 831-848

[12]Hata S, Matsuoka M. 1987. Immunological studies onpyruvate orthophosphate dikinase in C3 plants. Plantand Cell Physiology, 28, 635-641

[13]Hatch M D, Slack C R. 1966. Photosynthesis by sugarcaneleaves. A new carboxylation reaction and thepathway of sugar formation. Journal of Biochemistry,101, 103-111

[14]Hedley C L, Harvey D M, Keely R J. 1975. Role of PEPcarboxylase during seed development in Pisum sativum.Nature, 258, 352-354

[15]Hibberd J M, Quick W P. 2002. Characteristics of C4photosynthesis in stems and petioles of C3 floweringplants. Nature, 415, 451-454

[16]Hibberd J M, Sheehy J E, Langdale J A. 2008. Using C4photosynthesis to increase the yield of rice-rationaleand feasibility. Current Opinion in Plant Biology, 11,228-231

[17]Hudspeth R L, Grula J W, Dai Z, Edwards G E, Ku M S B.1992. Expression of maize phosphoenolpyruvatecarboxylase in transgenic tobacco. Effects onbiochemistry and physiology. Plant Physiology, 98,458-464

[18]Jiao J, Chollet R. 1991. Posttranslational regulation ofphosphoenolpyruvate carboxylase in C4 andCrassulacean acid metabolism plants. Plant Physiology,95, 981-985

[19]Kogami H, Shono M, Koike T, Yanagisawa S, Izui K,Sentoku N, Tanifuji S, Uchirniya H, Toki S. 1994.Molecular and physiological evaluation of transgenictobacco plants expressing a maize phosphoenolpyruvatecarboxylase gene under the control of the cauliflowermosaic virus 35S promoter. Transgenic Research, 3,287-296

[20]Ku M S B, Agarie S, Nomura M, Fukayama H, Tsuchida H,Ono K, Hirose S, Toki S, Miyao M, Matsuoka M. 1999.High level expression of maize phosphoenolpyruvatecarboxylase in transgenic rice plants. NatureBiotechnology, 17, 76-80

[21]Ku M S B, Kano M Y, Matsuoka M. 1996. Evolution andexpression of C4 photosynthesis genes. PlantPhysiology, 111, 947-957

[22]Latzko E, Kelly G J. 1983. The many-faceted function ofphosphoenolpyruvate carboxylase in C3 plants.Physiological Vegetable, 21, 805-813

[23]Laval M D, Farineau J, Diamond J. 1977. Light versus darkcarbon metabolism in cherry tomato fruits. PlantPhysiology, 60, 872-876

[24]Lepiniec L, Vidal J, Chollet R, Gadal P, Crétin C. 1994.Phosphoenolpyruvate carboxylase: structure,regulation and evolution. Plant Science, 99, 111-124

[25]Matsuoka M, Nomura M, Agarie S, Miyao-Tokutomi M,Ku M S B. 1998. Evolution of C4 photosynthetic genesand over expression of maize C4 genes in rice. Journalof Plant Research, 111, 333-337

[26]Marris P F, Savard M E, Ward E W B. 1991. Identificationand accumulation of isoflavone glucosides in soybeanleaves and hypocotyls in resistance response tophysiological and molecular. Journal of PlantPathology, 39, 229-244

[27]Meyer A O, Kelly G J, Latzko E. 1982. Pyruvateorthophosphate dikinase from the immature grain ofcereal grasses. Plant Physiology, 69, 7-10

[28]Nomura M, Higuchi T, Ishida Y, Ohta S, Komari T, ImaizumiN, Miyao T M, Matsuoka M, Tajima S. 2005. Differentialexpression pattern of C4 bundle sheath expression genesin rice, a C3 plant. Plant and Cell Physiology, 46, 754-761

[29]Nutbeam A R. 1976. Evidence for a C. photosynthesis inbarly pericarp tissue. Biochemical and BiophysicalResearch Communications, 70, 1198-1203

[30]Parvathi K, Bhagwat A S, Ueno Y, Izui K, Raghavendra A S.2000. Illumination increases the affinity ofphosphoenolpyruvate carboxylase to bicarbonate inleaves of a C4 plant, Amaranthus hypochondriacus.Plant and Cell Physiology, 41, 905-910

[31]Patel M, Berry J O. 2008. Rubisco gene expression in C4plants. Journal of Experimental Botany, 59, 1625-1634

[32]Rosche E, Streubel M, Westhoff P. 1994. Primary structureof the photosynthetic pyruvate orthophosphatedikinase of the C3 plant Flaveria pringlei and expressionanalysis of pyruvate orthophosphate dikinasesequences in C3, C3-C4 and C4 Flaveria species. PlantMolecular Biology, 26, 763-769

[33]Salahas G, Manetas Y, Gavalas N A. 1990. Assaying forpyruvate orthophosphate dikinase activity: necessaryprecautions with phosphoenolpyruvate carboxylase ascoupling enzyme. Photosynthesis Research, 24, 183-188

[34]Sheen J. 1999. C4 gene expression. Annual Review of PlantPhysiology Plant Molecular Biology, 50, 187-217

[35]Svensson P, Blasing O E, Westho V P. 2003. Evolution ofC4 phosphoenolpyruvate carboxylase. Archives ofBiochemistry and Biophysics, 414, 180-188

[36]Wang J L, Klessig D F, Berry J O. 1992. Regulation of C4gene expression in developing amaranth leaves. ThePlant Cell, 4, 173-184

[37]Wang J L, Turgeon R, Carr J P, Berry J O. 1993. Carbonsink-to-source transition is coordinated withestablishment of cell-specific gene expression in a C4plant. The Plant Cell, 5, 289-296

[38]Wirth E, Kelly G J, Fischbeck G, Latzko E. 1977. Enzymeactivities and products of CO2 fixation in variousphotosynthetic organs of wheat and oat. Zeitschriftfür Pflanzenphysiology, 82, 78-87

[39]Yuu T, Hiromori A, Naomi K, Masako O, Hideo H. 2000.Aberrant chloroplasts in transgenic rice plantsexpressing a high level of maize NADP-dependent malicenzyme. Planta, 211, 265-274

[40]Zhang B J, Chen Q Z, Hua C, Zhou F, Zhou Q C, Jiao D M.2009. Response of gas exchange and water use efficiencyto light intensity and temperature in transgenic riceexpressing PEPC and PPDK genes. AgriculturalSciences in China, 11, 1312-1320
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