Sains Malaysiana 47(2)(2018):
235-242
http://dx.doi.org/10.17576/jsm-2018-4702-04
Activities of C4 Photosynthetic Pathway Enzymes in Different Bread Wheat Genotypes
under Field Conditions
(Aktiviti Laluan Fotosintetik Enzim C4 dalam Genotip Gandum yang Pelbagai pada Keadaan Lapangan)
Bachir Goudia Daoura1,
Iqbal Saeed1,2, Quanhao Song1,
Yang Yang1, Liang Chen1
& Yin-Gang Hu1, 3*
1State Key Laboratory of Crop Stress Biology for
Arid Areas, College of Agronomy, Northwest A&F University,
Yangling, Shaanxi, 712100, China
2Nifa, Po Box 446, Tarnab, Peshawar, Kp, Pakistan
3Institute of Water Saving Agriculture in Arid
Regions of China, Northwest A&F University
Yangling, Shaanxi, 712100, China
Received: 2 February 2017/Accepted: 28 July 2017
ABSTRACT
The activities of key C4 photosynthetic enzymes including phosphoenolpyruvate carboxylase (PEPcase),
NADP-malic enzyme (NADP-ME), malate dehydrogenase (MDH) and pyruvate phosphate
dikinase (PPDK) were assayed in flag leaves at three major growth stages
(heading, anthesis and grain filling) among 59 winter wheat genotypes grown in
field conditions. All C4 enzymes expressed in the flag leaves and
their activation showed a wide range of variation in relation to different
growth stages in all the genotypes. PEPCase, NADP-ME and MDH displayed the
highest mean activities of 1.018, 0.758 and 0.731 µmol. min-1.mg-1 protein at heading stage, respectively; while PPDK showed
the highest mean activity (0.888 µmol. min-1.mg-1 protein)
at grain filling stage. The activities of
PEPcase and PPDK were higher at heading stage, decreased at anthesis and again increased at grain filling stage,
while NADP-ME and MDH exhibited a decreasing trend at the three stages. The
results of the current study could be valuable and useful for wheat researchers
in improving photosynthetic capacity of wheat.
Keywords: C4 enzymes; flag leaf;
photosynthetic efficiency; transgenic plants; wheat
ABSTRAK
Aktiviti enzim fotosintetik C4 yang
utama termasuk fosfoenol piruvat karboksilase (PEPcase),
enzim NADP-malik (NADP-ME), malat dehidrogenase (MDH) dan piruvat fosfat
dikinase (PPDK) diasai pada daun bendera dalam tiga peringkat pertumbuhan utama (kepala, antesis dan isi
bijirin) dalam kalangan 59 genotip gandum musim sejuk yang ditanam dalam
keadaan lapangan berbeza. Semua enzim C4 dinyatakan pada daun bendera dan pengaktifan mereka menunjukkan pelbagai
variasi berhubung dengan peringkat pertumbuhan yang berbeza di semua genotip. PEPCase, NADP-ME dan MDH menunjukkan aktiviti min tertinggi
sebanyak 1.018, 0.758 dan 0.731 μmol. protein min-1.mg-1 di peringkat tajuk, masing-masing; manakala
PPDK menunjukkan aktiviti min tertinggi (0.888 μmol. min-1.mg-1 protein) pada peringkat pengisian bijian. Kegiatan PEPcase dan PPDK lebih
tinggi pada peringkat tajuk, menurun pada antesis dan sekali lagi meningkat
pada peringkat pengisian bijirin, sementara NADP-ME dan MDH menunjukkan
penurunan pada tiga tahap. Keputusan kajian ini bernilai dan bermanfaat untuk
penyelidik gandum dalam meningkatkan kapasiti fotosintesis gandum.
Kata kunci: Daun bendera; enzim C4; gandum; kecekapan fotosintesis; tumbuhan transgenik
REFERENCES
Ana-Luz, B.C., Carlos, M.J., Jose, D.M.G. & Rosario,
M.C. 1994. Phosphoenolpyruvate carboxylase and malic enzyme in
leaves of two populations of maize differing in grain yield. J. Plant Physiol.143: 15-20.
Babayev, H.G., Bayramov,
Sh.M., Mehvaliyeva, U.A., Aliyeva, M.N., Guliyev, N.M., Huseynova, I.M. &
Aliyev, J.A. 2013. Activities of C4-photosynthetic
enzymes in different wheat genotypes under continuous soil drought conditions. J. Biochem. Res.1: 7-16.
Christin, P.A.,
Freckleton, R.P. & Osborne, C.P. 2010. Can phylogenetics identify C4 origins
and reversals? Trends Ecol. Evol. 25: 403-409.
Drincovich,
M.F., Casati, P. & Andreo, C.S. 2001. NADP-malic enzyme from plants: A ubiquitous enzyme involved in
different metabolic pathways. FEBS
Letters 490: 1-6.
Forrester, R.L., Wataji,
L.J., Silverman, D.A. & Pierre, K.J. 1976. Enzymatic
method for determination of CO2 in serum Clin. Chem. 22: 243-245.
Fukayama,
H., Tsuchida, H., Agarie, S., Nomura, M., Onodera, H., Ono, K., Lee, B.,
Hirose, S., Toki, S. & Ku, M.S. 2001. Significant
accumulation of C4-specific pyruvate, orthophosphate dikinase in a C3 plant, rice. Plant Physiol.127:
1136-1146.
Gehlen, J., Panstruga, R., Smets, H., Merkelbach, S.,
Kleines, M., Porsch, P., Fladung, M., Becker, I., Rademacher, T. & Hausler,
R.E. 1996. Effects of altered phosphoenolpyruvate carboxylase
activities on transgenic C3 plant Solanum tuberosum. Plant Mol.
Biol. 32: 831-848.
Gonzalez, D.H.,
Iglesias, A.A. & Andeo, C.S. 1984. On the regulation of phosphoenolpyruvate
carboxylase activity from maize leaves by L-malate. Effect of
pH. J. Plant Physiol. 116:
425-434.
Han,
L.L., Xu, W.G., Hu, L.,
Li, Y., Qi, X.L., Zhang, J.H., Zhang, H.F. & Wang, Y.X. 2013. Preliminary study on the physiological characteristics of
transgenic wheat with maize C4-pepc gene in field conditions. Cereal Res. Commun. 42: 1-11.
Hatch,
M.D. 1987. C4 photosynthesis: A unique blend of
modified biochemistry, anatomy and ultrastructure. Bioch. Bioph. Acta 895: 81-106.
Hibberd, J.M. &
Quick, W.P. 2002. Characteristics of C4 photosynthesis in stems and petioles of C3 flowering plants. Nature 415: 451-454.
Hu, L., Li, Y., Xu, W.G., Zhang, Q.C., Zhang, L., Qi,
X.L. & Dong, H.B. 2012. Improvement of the
photosynthetic characteristics of transgenic wheat plants by transformation with
the maize C4 phosphoenolpyruvate carboxylase gene. Plant Breed. 131: 385-391.
Huang, S.S., Li, C.S.,
Yang, M.L., Li, W.B. & Wang, J.A. 2013. Relationships
between C4 enzyme activities and yield in soybeans (Glycine max (L.)
Merr.). J. Integr. Agri. 12: 406-413.
Jiao, D., Huang, X., Li, X., Chi, W., Kuang, T., Zhang,
Q., Ku, M.S. & Cho, D. 2002. Photosynthetic characteristics and
tolerance to photo-oxidation of transgenic rice expressing C4 photosynthesis enzymes. Photosynth. Res. 72: 85-93.
Ku, M.S., Agarie, S.,
Nomura, M., Fukayama, H., Tsuchida, H., Ono, K., Hirose, S., Toki, S., Miyao, M. & Matsuoka, M. 1999. High-level
expression of maize phosphoenolpyruvate carboxylase in transgenic rice plants. Nat. Biotechnol. 17:
76-80.
Ku,
M.S., Cho, D., Ranade, U., Hsu, T.P., Li, X.,, D.M, Ehleringer, J. & Miyao, M. 2000. Photosynthetic
performance of transgenic rice plants over-expressing maize C4 photosynthesis enzymes. Stud. Plant Sci. 7: 193-204.
Lin, H., Yan, L.,
WeiGang, X., QingChen, Z., Lei, Z., Xueli,
Q. & Haibin, D. 2012. Improvement of the photosynthetic
characteristics of transgenic wheat plants by transformation with the maize C4 phosphoenolpyruvate carboxylase gene. Plant
Breed. 131: 385-391.
López-Calcagno,
P.E., Moreno, J., Cedeño, L., Labrador, L., Concepción, J.L. & Avilán, L.
2009. Cloning, expression and biochemical characterization of
mitochondrial and cytosolic malate dehydrogenase from Phytophthora infestans. Mycol. Res. 113: 771-781.
Ludwig, M. 2012. Carbonic anhydrase and the molecular evolution of C4 photosynthesis. Plant Cell Environ. 35: 22–37.
Matsuoka, M., Nomura, M., Agarie, S., Miyao-Tokutomi, M.
& Ku, M.S.B. 1998. Evolution of C4 photosynthetic genes and over expression of maize C4 genes in rice. J. Plant Res. 111: 333-337.
Miyao,
M. 2003. Molecular evolution and genetic engineering of C4 photosynthetic enzymes.J. Exp. Bot. 54: 179-189.
Murata,
Y. 1981. Dependence of potential productivity
and efficiency for solar energy utilization on leaf photosynthetic
capacity in crop species. Japan. J.
Crop Sci. 50: 223-232.
Reynolds,
M.P., Delgado, M.I., Gutierrez-Rodriguez, M. & Larque-Saavedra, A. 2000. Photosynthesis of wheat
in a warm, irrigated environment I: Genetic diversity and crop productivity. Field Crops Res. 66: 37-50.
Riccardi,
F., Gazeau, P., Vienne, D. & Zivy, M. 1998. Protein changes in
response to progressive water deficit in maize. Plant Physiol. 117: 1253-1263.
Surridge,
C. 2002. Agricultural biotech: The
rice squad. Nature 416: 576–578.
Takeuchi, Y., Akagi, H., Kamasawa, N., Osumi, M. &
Honda, H. 2000. Aberrant chloroplasts in transgenic
rice plants expressing a high level of maize NADP-dependent malic enzyme. Planta 211: 265-274.
Taniguchi,
Y., Ohkawa, H., Masumoto, C., Fukuda, T., Tamai, T., Lee, K., Sudoh, S.,
Tsuchida, H., Sasaki, H. & Fukayama, H. 2008. Overproduction of C4 photosynthetic
enzymes in transgenic rice plants: An approach to introduce the C4-like
photosynthetic pathway into rice. J. Exp.
Bot. 59: 1799-1809.
Tolley, B.J., Sage, T.L., Langdale, J.A. & Hibberd,
J.M. 2012. Individual maize chromosomes in the C3 plant
oat can increase bundle sheath cell size and vein density. Plant Physiol. 159: 1418-1427.
Tsuchida,
H., Tamai, T., Fukayama, H., Agarie, S., Nomura, M., Onodera, H., Ono, K.,
Nishizawa, Y., Lee, B., Hirose, S., Toki, S., Ku, M.S.B., Matsuoka, M. & Miyao,
M. 2001. High level expression of C4-specific
NADP-Malic enzyme in leaves and impairment of photoautotrophic growth in a C3 plant, rice. Plant Cell Physiol. 42:
138-145.
Umeda,
M., Hare, C., Matsubayashi, Y., Li, H., Tadokoro, F., Aotsuka, S. & Uchimiya, H.
1994. Expressed sequence tags from cultured cell of rice (Oryza sativa L.)
under stressed conditions: Analysis of genes engaged
in ATP-generating pathway. Plant Mol. Biol. 25: 469-478.
Wang,
Q., Lu, C.M., Zhang, Q.D., Hao, N.B., Ge, Q.Y.,
Dong, F.Q., Bai, K.Z. & Kuang T.Y. 2002. Characteristics
in photosynthesis, photoinhibition and C4 pathway enzymes in a
super-high-yield LYPJ. Sci. China C-life Sci. 32: 481-487.
Wang, Y.M., Xu, W.G., Hu, L., Zhang, L.,
Li, Y. & Du, X.H. 2012. Expression of maize gene encoding C4-pyruvate
orthophosphate dikinase (PPDK) and C4-phosphoenolpyruvate
carboxylase (PEPC) in transgenic Arabidopsis. Plant Mol. Biol. Report 30: 1367-1374.
Wu, Q., Xu, W.G., Li, Y., Qi, X.L., Hu, L.,
Zhang, L. & Han, L.L. 2011. Physiological
characteristics of photosynthesis in transgenic wheat with maize C4-PEPC
gene under field conditions. Acta Agr.
Sin. 37: 2046-2052.
Yang, C.W., Lin, G.Z., Peng, C.L., Chen, Y.Z. & Ou,
Z.Y. 2003. Changes in the activities of C4 pathway
enzymes and stable carbon isotope discrimination in flag leaves of
super-high-yield hybrid rice. Acta Bot.
Sin. 45: 1261-1265.
Zhang, B.J., Ling, L.L., Chen, Q.Z., Hua, C. & Jiao, D.M. 2009. A key limited factor ATP of constructing C4-like rice. Acta Agri. Bor. Sin. 24: 17-22.
Zhang, C.J., Chen, L.,
Shi, D.W., Chen, G.X., Lu, C.G., Wang, P., Wang, J., Chu, H.J., Zhou, Q.C.,
Zuo, M. & Sun, L. 2007. Characteristics of ribulose-1,5-bisphosphate
carboxylase and C4 pathway key enzymes in flag leaves of a
super-high-yield hybrid rice and its parents during the reproductive stage. S. Afr. J. Bot. 73: 22-28.
Zhang, H.F., WeiGang,
X., HuiWei, W., Lin, H., Yan, L., Qi, X., Zhang,
L., Li, C. & Hua, X. 2014. Pyramiding expression of
maize genes encoding phosphoenolpyruvate carboxylase (PEPC) and pyruvate
orthophosphate dikinase (PPDK) synergistically improve the photosynthetic
characteristics of transgenic wheat. Protoplasma 251: 1163-1173.
Zhang, J.H., Xu, W.G., Wang, H.W., Li, Y.,
Hu, L., Han, L.L. & Zhang, H.F. 2012. Molecular characteristics and photosynthetic property of the
transgenic wheat expressing a maize C4-type PEPC gene. J. Triticeae Crops 32: 1043-1048.
Zheng, T.C., Zhang, X.K., Yin, G.H., Wang, L.N., Han, Y.L., Chen, L.,
Huang, F., Tang, J.W., Xia, X.C. & He, Z.H. 2011. Genetic gains in grain
yield, net photosynthesis and stomatal conductance achieved in Henan Province
of China between 1981 and 2008. Field
Crop Res. 122: 225-233.
*Corresponding author; email: Huyingang@Nwsuaf.Edu.Cn
|