Chinese Journal of Plant Ecology >
A REVIEW OF ADAPTABLE VARIATIONS AND EVOLUTION OF PHOTOSYNTHETIC CARBON ASSIMILATING PATHWAY IN C3 AND C4 PLANTS
Received date: 2008-01-16
Accepted date: 2008-05-15
Online published: 2009-01-30
Three photosynthetic pathways are used by plants: C3, which most plants use, C4 and crassulacean acid metabolism (CAM). C3 is the ancestral pathway, with C4 and CAM representing recently diverged forms. We conclude that the variation and evolution of photosynthetic pathway of C3 and C4 are adaptations to environmental stresses. First, we discuss the evolutional future of photosynthetic pathways. It has been suggested that low atmosphere CO2, enhanced temperatures, drought and salinity are external drivers of C4 photosynthetic evolution. Second, we analyze the possibility of evolution from C3 to C4. The polyphyletic evolution of the C4 pathway suggests that the transition from C3 to C4 was relatively simple. This suggestion is supported by the observation that both C3 and C4 plants possess inherent plasticity in their photosynthetic characteristics. The stress causing the shift from C3 to C4 was involved in the environmental regulation of plants, and the C4 pathway in C3 plants evolved as an adaptation. The environmental stresses may have involved plant capacities for survivorship and competition in arid areas. Third, we present a simplistic model of the main phases of C4 photosynthetic evolution and discuss the variation and evolution of C3 and C4 photosynthetic carbon assimilating pathways. Evolution was not directly to C4 photosynthesis, so each step had to be stable, beginning with numerous preconditions needed for an evolutionary lineage to begin evolving C4 characteristics. A current complication of C4 photosynthetic evolution is global climate change and human manipulation of the biosphere. It is possible that C4 photosynthesis can be used to resist adversity and increase the yield of C3 crops. In conclusion, study of the evolution of photosynthetic pathway in plants provided insight into the photosynthetic physiology of plants under stress and provided new theory to reconstruct vegetation, enhance crop yield, and explain adaptation of C3 species in arid areas.
Key words： C3 plants; C4 plants; C4 pathway; drought; adaptable evolution
GONG Chun-Mei, NING Peng-Bo, WANG Gen-Xuan, LIANG Zong-Suo . A REVIEW OF ADAPTABLE VARIATIONS AND EVOLUTION OF PHOTOSYNTHETIC CARBON ASSIMILATING PATHWAY IN C3 AND C4 PLANTS[J]. Chinese Journal of Plant Ecology, 2009 , 33(1) : 206 -221 . DOI: 10.3773/j.issn.1005-264x.2009.01.023
| [1] | Ali S, Taylor WC (2001). The 3′ non-coding region of C4 photosynthesis gene increases transgene expression when combined with heterologous promoters. Plant Molecular Biology, 46, 325-333. |
| [2] | Badger MR, Price GD (1992). The CO2 concentrating mechanism in cyanobacteria and microalgae. Physiologia Plantarum, 84, 606-615. |
| [3] | Biehler K, Fock H (1996). Evidence for the contribution of the Mehler-peroxidase reaction in dissipating excess electrons in drought stressed wheat. Plant Physiology, 112, 265-272. |
| [4] | Bjorkman O, Nobs M, Pearcy R, Boynton J, Berry J (1971). Characteristics of hybrids between C3 and C4 species of Atriplex. In: Hatch MD, Osmond CB, Slatyer RO eds. Photosynthesis and Photorespiration. Wiley-Interscience, New York, 105-119. |
| [5] | Bl?sing OE, Ernst K, Streubel M, Westhoff P, Svensson P (2002). The non-photosynthetic phosphoenolpyruvate carboxylases of the C4 dicot Flaveria trinervia - implications for the evolution of C4 photosynthesis. Planta, 215, 448-456. |
| [6] | Bota J, Medrano H, Flexas J (2004). Is photosynthesis limited by decreased Rubisco activity and RuBP content under progressive water stress? New Phytologist, 162, 671-681. |
| [7] | Bowes G (1993). Facing the inevitable: plants and increasing atmospheric CO2. Annual Review of Plant Physiology and Plant Molecular Biology, 44, 309-332. |
| [8] | Bowes G, Salvucci ME (1989). Plasticity in the photosynthetic carbon metabolism of submerged aquatic macrophytes. Aquatic Botany, 34, 233-266. |
| [9] | Brown HA (1999). Agronomic implications of C4 photosynthesis. In: Sage RF, Monson RK eds. C4 Plant Biology. Academic Press, San Diego, CA, USA, 473-508. |
| [10] | Brown RH, Hattersley PW (1989). Leaf anatomy of C3-C4 species as related to evolution of C4 photosynthesis. Plant Physiology, 91, 1543-1550. |
| [11] | Brown NJ, Parsley K, Hibberd JM (2005). The future of C4 research — maize, Flaveria or Cleome? Trends in Plant Science, 10, 215-221. |
| [12] | Carolin RC, Jacobs SWL, Vesk M (1975). Leaf structure in Chenopodiaceae. Botanische Jahrbücher für Systematische Pflanzengeschichte und Pflanzengeographie, 95, 226-255. |
| [13] | Carolin RC, Jacobs SWL, Vesk M (1978). Kranz cells and mesophyll in Chenopodiaceae. Australian Journal of Plant Physiology, 26, 683-698. |
| [14] | Cheng SH, Moore BD, Edwards GE, Ku MSB (1988). Photosynthesis in Flaveria brownii, a C4-like species. Plant Physiology, 87, 867-873. |
| [15] | Cheng SH, Moore BD, Wu J, Edwards GE, Ku MSB (1989). Photosynthetic plasticity in Flaveria brownii. Growth irradiance and the expression of C4 photosynthesis. Plant Physiology, 89, 1129-1135. |
| [16] | Chollet R, Vidal J, O’Leary MH (1996). Phosphoenolpyruvate carboxylase: a ubiquitous, highly regulated enzyme in plants. Annual Review of Plant Physiology and Plant Molecular Biology, 47, 273-298. |
| [17] | Cornic G, Fresneau C (2002). Photosynthetic carbon reduction and carbon oxidation cycles are the main electron sinks for photosystem II activity during a mild drought. Annals of Botany, 89, 887-894. |
| [18] | Cushman JC, Bohnert HJ (2000). Genomics approaches to plant stress. Current Opinion in Plant Biology, 3, 117-124. |
| [19] | Dengler NG, Nelson T (1999). Leaf structure and development in C4 plants. In: Sage RF, Monson RK eds. C4 Plant Biology. Academic Press, San Diego, CA, USA, 133-172. |
| [20] | Doebley J, Lukens L (1998). Transcriptional regulators and the evolution of plant form. The Plant Cell, 10, 1075-1082. |
| [21] | Drincovich MF, Casati P, Andreo CS, Chessin SJ, Franceschi VR, Edwards GE, Ku MSB (1998). Evolution of C4 photosynthesis in Flaveria species: isoforms of NADP-malic enzyme. Plant Physiology, 117, 733-744. |
| [22] | Duffus CM, Rosie R (1973). Some enzyme activities associated with the chlorophyll containing layers of the immature barley pericarp. Planta, 111, 219-226. |
| [23] | Edwards GE, Furbank RT, Hatch MD, Osmond CB (2001). What does it take to be C4? Lessons from the evolution of C4 photosynthesis. Plant Physiology, 125, 46-49. |
| [24] | Edwards GE, Ku MSB (1987). Biochemistry of C3-C4 intermediates. In: Stumpf PK, Conn EE eds. The Biochemistry of Plants, Vol. 10. Academic Press, New York, 275-325. |
| [25] | Edwards GE, Walker DA (1983). C3,C4: Mechanisms, and Cellular and Environmental Regulation of Photosynthesis. Blackwell Scientific Publications, Oxford. |
| [26] | Ehleringer JR, Cerling TE, Helliker BR (1997). C4 photosynthesis, atmospheric CO2 and climate. Oecologia, 112, 285-299. |
| [27] | Feng L (封玲) (2007). The changes of forest resource and its influence to ecological environment in Manasi River Basin of Xinjiang. Ecology and Environment (生态环境), 2, 372-376. (in Chinese with English abstract) |
| [28] | Gillon J, Yakir D (2001). Influence of carbonic anhydrase activity in terrestrial vegetation on the 18O content of atmospheric CO2. Science, 291, 2584-2587. |
| [29] | Gimenez C, Mitchell VJ, Lawlor DW (1992). Regulation of photosynthetic rate of two sunflower hybrids under water stress. Plant Physiology, 98, 516-524. |
| [30] | Gong CM, Gao XW, Cheng DL, Wang GX (2006). C4 photosynthetic characteristics and antioxidative protection of C3 desert shrub Hedysarum scoparium in Northwest China. Pakistan Journal of Botany, 38, 647-661. |
| [31] | Gowik U, Burscheidt J, Akyildiz M, Schlue U, Koczor M, Streubel M (2004). cis-Regulatory elements for mesophyll specific gene expression in the C4 plant Flaveria trinervia, the promoter of the C4 phosphoenolpyruvate carboxylase gene. The Plant Cell, 16, 1077-1090. |
| [32] | Gunasekera D, Berkowitz GA (1993). Use of transgenic plants with ribulose-1,5-bisphosphate carboxylase/oxygenase antisense DNA to evaluate the rate limitation of photosynthesis under water stress. Plant Physiology, 103, 629-635. |
| [33] | Guy RD, Reid DM, Krouse HR (1986). Factors affecting 13C/ 12C ratios of inland halophytes. I. Controlled studies on growth and isotopic composition of Puccinellia nuttalliana. Canadian Journal of Botany, 64, 2693-2699. |
| [34] | Han JM (韩家懋), Wang GA (王国安), Liu DS (刘东生) (2002). Appearance of C4 plants and global changes. Earth Science Frontiers (地学前缘), 9, 233-243. (in Chinese with English abstract) |
| [35] | Hatch MD (1987). C4 photosynthesis: a unique blend of modified biochemistry, anatomy and ultrastructure. Biochimica et Biophysica Acta, 895, 81-106. |
| [36] | Hatch MD (1992). C4 photosynthesis: an unlikely process full of surprises. Plant & Cell Physiology, 33, 333-342. |
| [37] | Hatch MD, Slack CR (1966). Photosynthesis in sugar-cane leaves: a new carboxylation reaction and the pathway of sugar formation. Biochemical Journal, 101, 103-111. |
| [38] | Hayes JM (1994). Global methanothophy at the Archean-Proterozoic transition. In: Bengston S ed. Early Life on Earth. Columbia University Press, New York, 220-236. |
| [39] | Hegerl GC, Hasselmann K, Cubasch U, Mitchell JFB, Roeckner E, Voss R, Waszkewitz J (1997). Multi-fingerprint detection and attribution analysis of greenhouse gas, greenhouse gas-plus-aerosol and solar forced climate change. Climate Dynamics, 13, 613-634. |
| [40] | Hibberd JM, Quick WP (2002). Characteristics of C4 photosynthesis in stems and petioles of C3 flowering plants. Nature, 415, 451-454. |
| [41] | Hibberd JM, Sheehy JE, Langdale JA (2008). Using C4 photosynthesis to increase the yield of rice—rationale and feasibility. Current Opinion in Plant Biology, 11, 228-231. |
| [42] | Hudson GS, Mahon JD, Anderson PA, Gibbs MJ, Badgers MR, Andrews TJ, Whitfeld PR (1990). Comparisons of rbcL genes for the large subunit of ribulose-bisphosphate carboxyase from closely related C3 and C4 plant species. Journal of Biological Chemistry, 265, 808-814. |
| [43] | Huxman TE, Monson RK (2003). Stomatal responses of C3, C3-C4 and C4 Flaveria species to light and intercellular CO2 concentration: implications for the evolution of stomatal behaviour. Plant, Cell and Environment, 26, 313-322. |
| [44] | IDAG (International Ad Hoc Detection and Attribution Group) (2005). Detecting and attributing external influences on the climate system: a review of recent advances. Journal of Climate, 18, 1291-1314. |
| [45] | Imaizumi N, Samejima M, Ishihara K (1997). Characteristics of photosynthetic carbon metabolism of spikelets in rice. Photosynthesis Research, 52, 75-82. |
| [46] | Izui K, Matsumura H, Furumoto T, Kai Y (2004). Phosphoenolpyruvate carboxylase: a new era of structural biology. Annual Review of Plant Biology, 55, 69-84. |
| [47] | Jordan DB, Ogren WL (1984). The CO2/O2 specificity of ribulose-1, 5-bisphosphate concentration, pH and temperature. Planta, 161, 308-313. |
| [48] | Keeley JE (1998). C4 photosynthetic modifications in the evolutionary transition from land to water in aquatic grasses. Oecologia, 116, 85-97. |
| [49] | Keeley JE (1999). Chaparral. In: Barbour MB, Billings WD eds. North American Terrestrial Vegetation. Cambridge University Press, Cambridge, 201-251. |
| [50] | Kellogg EA (1999). Phylogenetic aspects of the evolution of C4 photosynthesis. In: Sage RF, Monson RK eds. C4 Plant Biology. Academic Press, San Diego, CA, USA, 411-444. |
| [51] | Kicheva MI, Tsonev TD, Popova LP (1994). Stomatal and non-stomatal limitations to photosynthesis in two wheat cultivars subjected to water stress. Photosynthetica, 30, 107-116. |
| [52] | Kirchhamer CV, Yuh CH, Davidson EH (1996). Modular cis-regulatory organization of developmentally expressed genes: two genes transcribed territorially in the sea urchin embryo, and additional examples. Proceedings of the National Academy of Sciences of the United States of America, 93, 9322-9328. |
| [53] | Kocacinar F, Sage RF (2003). Photosynthetic pathway alters xylem structure and hydraulic function in annual plants. Plant, Cell and Environment, 26, 2015-2026. |
| [54] | Ku MSB, 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. Nature Biotechnology, 17, 76-80. |
| [55] | Ku MSB, Cho D, Ranade U, Hsu TP, Li X, Jiao DM, Ehleringer J, Miyao M, Matsuoka M (2000). Photosynthetic performance of transgenic rice plants overexpressing maize C4 photosynthesis enzymes. In: Sheehy JE, Mitchell PL, Hardy B eds. Redesigning of Rice Photosynthesis to Increase Yield. Elsevier Science Publishers, Amsterdam, The Netherlands, 193-204. |
| [56] | Ku MSB, Wu JR, Dai ZY, Scott RA, Chu C, Edwards GE (1991). Photosynthetic and photorespiratory characteristics of Flaveria species. Plant Physiology, 96, 518-528. |
| [57] | Laetsch WM (1974). The C4 syndrome: a structural analysis. Annual Review of Plant Physiology, 25, 27-52. |
| [58] | Lai LB, Tausta L, Nelson TM (2002). Differential regulation of transcripts encoding cytosolic NADP-malic enzyme in C3 and C4 Flaveria species. Plant Physiology, 128, 140-149. |
| [59] | Langdale JA, Taylor WC, Nelson T (1991). Cell-specific accumulation of maize phosphoenolpyruvate carboxylase is correlated with demethylation at a specific site greater than 3 kb upstream of the gene. Molecular Genetics and Genomics, 225, 49-55. |
| [60] | Latzko E, Kelly GJ (1983). The many-faceted function of phosphoenolpyruvate carboxylase in C3 plant. Physiologie Vegetale, 21, 805-815. |
| [61] | Lawlor DW (1995). The effects of water deficit on photosynthesis. In: Smirnoff N ed. Environment and Plant Metabolism. Bios Scientific Publishers, Oxford, 129-160. |
| [62] | Lawlor DW (2002). Limitation to photosynthesis in water-stressed leaves: stomata vs. metabolism and the ATP. Annals of Botany, 89, 871-885. |
| [63] | Li WH (李卫华), Hao NB (郝乃斌), Ge QY (戈巧英), Zhang QD (张其德) (1999). Advances in study on C4 pathway in C3 plant. Chinese Bulletin of Botany (植物学通报), 16, 97-106. (in Chinese with English abstract) |
| [64] | Li WH (李卫华), Lu QT (卢庆陶), Hao NB (郝乃斌), Ge QY (戈巧英), Zhang QD (张其德), Jiang GM (蒋高明), Du WG (杜维广), Kuang TY (匡廷云) (2000). The relation between C4 pathway enzymes and PSII photochemical function in soybean. Acta Botanica Sinica (植物学报), 42, 689-692. (in Chinese with English abstract) |
| [65] | Li ZL (李正理), Li RA (李荣敖) (1981). Anatomical observation of assimilating branches of nine xerophytes in Gansu. Acta Botanica Sinica (植物学报), 23, 181-185. (in Chinese with English abstract) |
| [66] | Majumdar S, Ghosh S, Glick BR, Dumbroff EB (1991). Activities of chlorophyllase, phosphoenolpyruvate carboxylase and ribulose-1,5-biphosphate carboxylase in the primary leaves of soybean during senescence and drought. Physiologia Plantarum, 81, 473-480. |
| [67] | Marshall JS, Stubbs JD, Taylor WC (1996). Two genes encode highly similar chloroplastic NADP-malic enzymes in Flaveria. Plant Physiology, 111, 1251-1261. |
| [68] | Metcalfe CR, Chalk L (1979). Anatomy of the Dicotyledons, Vol. 1: Systematic Anatomy of the Leaf and Stem. Oxford Science Publishers, Oxford. |
| [69] | Miyao M (2003). Molecular evolution and genetic engineering of C4 photosynthetic enzymes. Journal of Experimental Botany, 54, 179-189. |
| [70] | Monson RK (2003). Gene duplication, neofunctionalization, and the evolution of C4 photosynthesis. International Journal of Plant Sciences, 164, S43-S54. |
| [71] | Monson RK, Teeri JA, Ku MSB, Gurevitch J, Mets LJ, Dudley S (1988). Carbon-isotope discrimination by leaves of Flaveria species exhibiting different amounts of C3- and C4-cycle co-function. Planta, 174, 145-151. |
| [72] | Monson RK (1999). The origins of C4 genes and evolutionary pattern in the C4 metabolic phenotype. In: Sage RF, Monson RK eds. C4 Plant Biology. Academic Press, San Diego, CA, USA, 377-410. |
| [73] | Monson RK, Rawsthorne S (2000). CO2 assimilation in C3-C4 intermediate plants. In: Leegood RC, Sharkey TD, von Caemmerer SC eds. Photosynthesis: Physiology and Metabolism. Advances in Photosynthesis and Respiration, Vol. 9. Kluwer Academic Publishers, Dordrecht, The Netherlands, 533-555. |
| [74] | Moore BD, Ku MSB, Edwards GE (1989). Expression of C4-like photosynthesis in several species of Flaveria. Plant, Cell and Environment, 112, 541-549. |
| [75] | Niu SL (牛书丽), Jiang GM (蒋高明), Li YG (李永庚) (2004). Environmental regulations of C3 and C4 plants. Acta Ecologica Sinica (生态学报), 24, 308-314. (in Chinese with English abstract) |
| [76] | Niu S, Li Z, Xia J, Han Y, Wu M, Wan S (2008). Climatic warming changes plant photosynthesis and its temperature dependence in a temperate steppe of northern China. Environmental and Experimental Botany, 63, 91-101. |
| [77] | Nomura M, Katayama K, Nishimura A, Ishida Y, Ohta S, Komari T, Miyao-Tokutomi M, Tajima S, Matsuoka M (2000). The light promoter of rbcS in a C3 plant (rice) directs organ-specific, light-dependent expression in a C4 plant (maize), but does not confer bundle sheath cell-specific expression. Plant Molecular Biology, 44, 99-106. |
| [78] | Pan RC (潘瑞炽), Dong YD (董愚得) (2001). Plant Physiology (植物生理学) 4th edn. Higher Education Press, Beijing, 91-95. (in Chinese) |
| [79] | Pan RC (潘瑞炽), Dong YD (董愚得) (2004). Plant Physiology (植物生理学) 5th edn. Higher Education Press, Beijing, 56-57, 84-86. (in Chinese) |
| [80] | Parry MAJ, Androlojc PJ, Khan S, Lea PJ, Keys AJ (2002). Rubisco activity: effects of drought stress. Annals of Botany, 89, 833-839. |
| [81] | Parry MAJ, Delgado E, Vadell J, Keys AJ, Lawlor DW, Medrano H (1993). Water stress and the diurnal activity of ribulose-1,5-bisphosphate carboxylase in field grown Nicotiana tabacum genotypes selected for survival at low CO2 concentrations. Plant Physiology and Biochemistry, 31, 113-120. |
| [82] | Portis AR (1992). Regulation of ribulose-1,5-bisphosphate carboxylase/oxygenase activity. Annual Review of Plant Physiology, 43, 415-422. |
| [83] | Pyankov VI, Artyusheva EG, Edwards GE, Black Jr CC, Soltis PS (2001). Phylogenetic analysis of tribe Salsoleae (Chenopodiaceae) based on ribosomal ITS sequences: implications for the evolution of photosynthesis types. American Journal of Botany, 88, 1189-1198. |
| [84] | Pyankov VI, Black Jr CC, Artyusheva EG, Voznesenskaya EV, Ku MSB, Edwards GE (1999). Features of photosynthesis in Haloxylon species of Chenopodiaceae that are dominant plants in Central Asian deserts. Plant & Cell Physiology, 40, 125-134. |
| [85] | Raghavendra AS (1980). Characteristics of plant species intermediate between C3 and C4 pathways of photosynthesis: their focus of mechanism and evolution of C4 syndrome. Photosynthetica, 14, 271-273. |
| [86] | Raven PH, Evert RF, Eichhorn SE (1992). Biology of Plants 5th edn. Worth Publishers, New York. |
| [87] | Rawsthorne S (1992). C3-C4 intermediate photosynthesis: linking physiology to gene expression. The Plant Journal, 2, 267-274. |
| [88] | Reiskind JB, Madsen TV, van Ginkel LC, Bowes G (1997). Evidence that inducible C4-type photosynthesis is a chloroplastic CO2-concentrating mechanism in Hydrilla, a submersed monocot. Plant, Cell and Environment, 20, 211-220. |
| [89] | Rosche E, Westhoff P (1995). Genomic structure and expression of the pyruvate, orthophosphate dikinase gene of the dicotyledonous C4 plant Flaveria trinervia(Asteraceae). Plant Molecular Biology, 29, 663-678. |
| [90] | Roth-Nebelsick A, Uhl D, Mosbrugger V, Kerp H (2001). Evolution and function of leaf venation architecture: a review. Annals of Botany, 87, 553-566. |
| [91] | Sage RF (2001). Environmental and evolutionary preconditions for the origin and diversification of the C4 photosynthetic syndrome. Plant Biology, 3, 202-213. |
| [92] | Sage RF (2004). The evolution of C4 photosynthesis. New Phytologist, 161, 341-370. |
| [93] | Sage RF (1999). Why C4 photosynthesis? In: Sage RF, Monson RK eds. C4 Plant Biology. Academic Press, San Diego, CA, USA, 3-16. |
| [94] | Sage RF, Wedin DA, Li MR (1999). The biogeography of C4 photosynthesis patterns and controlling factors. In: Sage RF, Monson RK eds. C4 Plant Biology. Academic Press, San Diego, CA, USA, 313-373. |
| [95] | Sayre RT, Kennedy RA, Pringnitz DJ (1979). Photosynthetic enzyme activities and localization in Mollugo verticillata population differing on the leaves of C3 and C4 cycle operations. Plant Physiology, 64, 293-299. |
| [96] | Sage RF, Kubien DS (2003). Quo vadis C4? An ecophysiological perspective on global change and the future of C4 plants. Photosynthesis Research, 77, 209-225. |
| [97] | Sch?ffner AR, Sheen J (1991). Maize rbcS promoter activity depends on sequence elements not found in dicot rbcS promoters. The Plant Cell, 3, 997-1012. |
| [98] | Schulze ED, Hall AE (1982). Stomatal responses, water loss and CO2 assimilation rates of plants in contrasting environments. In: Lange OL, Nobel PS, Osmond CB, Ziegler H eds. Physiological Plant Ecology II: Water Relations and Carbon Assimilation. Springer-Verlag, Berlin, 181-230. |
| [99] | Sharkey TD, Seemann JR (1989). Mild water stress effects on carbon-reduction-cycle intermediates, ribulose bis-phosphate carboxylase activity, and spatial homogeneity of photosynthesis in intact leaves. Plant Physiology, 89, 1060-1065. |
| [100] | Sheehy JE, Mitchell PL, Hardy B (2000). Redesigning Rice Photosynthesis to Increase Yields. Elsevier Science Publishers, Amsterdam, The Netherlands. |
| [101] | Sheen J (1999). C4 gene expression. Annual Review of Plant Physiology and Plant Molecular Biology, 50, 187-217. |
| [102] | Shields LM (1950). Leaf xeromorphy as related to physiological and structural influences. Botanical Review, 16, 299-340. |
| [103] | Soros CL, Dengler NG (2001). Ontogenetic derivation and cell differentiation in photosynthetic tissues of C3 and C4 Cyperaceae. American Journal of Botany, 88, 992-1005. |
| [104] | Stott PA (2003). Attribution of regional-scale temperature changes to anthropogenic and natural causes. Geophysical Research Letters, 30, 1724. |
| [105] | Svensson P, Blsing OE, Westhoff P (2003). Evolution of C4 phosphoenolpyruvate carboxylase. Archives of Biochemistry and Biophysics, 414, 180-188. |
| [106] | Tang AC, Kawamitsu Y, Kanechi M, Boyer JS (2002). Photosynthesis oxygen evolution of low water potential in leaf discs lacking an epidermis. Annals of Botany, 89, 861-870. |
| [107] | Taiz L, Zeiger E (1991). Plant Physiology. The Benjamin/Cammings Publishing Company Inc., Redwood City, CA, USA. |
| [108] | Takeda T, Ueno O, Samejima M, Ohtani T (1985). An investigation for the occurrence of C4 photosynthesis in the Cyperaceae from Australia. The Botanical Magazine Tokyo, 98, 393-411. |
| [109] | Teng NJ (滕年军), Chen T (陈彤), Ling JX (林金星) (2006). A review on responses of plant sexual reproduction to elevated CO2. Journal of Plant Ecology (Chinese Version) (植物生态学报), 30, 1054-1063. (in Chinese with English abstract) |
| [110] | Tett SFB, Stott PA, Allen MR, Ingram W, Mitchell J (1999). Causes of twentieth-century temperature change near the Earth’s surface. Nature, 339, 569-572. |
| [111] | Tezara W, Lawlor DW (1995). Effects of water stress on the biochemistry and physiology of photosynthesis in sunflower. In: Mathis P ed. Photosynthesis from Light to Biosphere, Vol Ⅳ. Kluwer Academy Publishers, Hague, The Netherlands, 625-628. |
| [112] | Tezara W, Mitchell VJ, Driscoll SP, Lawlor DW (1999). Water stress inhibits plant photosynthesis by decreasing coupling factor and ATP. Nature, 401, 914-917. |
| [113] | Toh H, Kawamura T, Izui K (1994). Molecular evolution of phosphoenolpyruvate carboxylase. Plant & Cell Physiology, 17, 31-43. |
| [114] | Ueno O (1998). Induction of Kranz anatomy and C4-like biochemical characteristics in a submerged amphibious plant by abscisic acid. The Plant Cell, 10, 571-583. |
| [115] | Ueno O, Samejima M, Muto S, Miyachi S (1988). Photosynthesis characteristics of an amphibious plant, Eleocharis vivipara: expression of C4 and C3 modes in contrasting environments. Proceedings of the National Academy of Sciences of the United States of America, 85, 719-728. |
| [116] | Uhl D, Mosbrugger V (1999). Leaf venation density as a climate and environmental proxy: a critical review and new data. Palaeogeography, Palaeoclimatology, Palaeoecology, 149, 15-26. |
| [117] | von Caemmerer S (2000). Biochemical Models of Leaf Photosynthesis. CSIRO Publishing, Collingwood, Australia. |
| [118] | Voznesenskaya EV, Franceschi KO, Freitag H, Edwards GE (2001). Kranz anatomy is not essential for terrestrial C4 plant photosynthesis. Nature, 414, 543-546. |
| [119] | Voznesenskaya EV, Franceschi VR, Kiirats O, Artyusheva EG, Freitag H, Edwards GE (2002). Evidence for C4 photosynthesis without Kranz anatomy in Bienertia cycloptera(Chenopodiaceae). The Plant Journal, 31, 649-662. |
| [120] | Wang ZP (王智平), Chen QS (陈全胜) (2005). Recently photosynthesized carbon allocation and turnover: a minor review of the literature. Acta Phytoecologica Sinica (植物生态学报), 29, 845-850. (in Chinese with English abstract) |
| [121] | Weiner H, Burnell JN, Woodrow IE, Heldt HW, Hatch MD (1988). Metabolite diffusion into bundle sheath cells from C4 plant. Plant Physiology, 88, 815-822. |
| [122] | Xin ZB (信忠保), Xu JX (许炯心), Zheng W (郑伟) (2007). The effect of climate change and human activity on variational cover of vegetation in Loess Plateau. Science in China Series D (中国科学 D 辑), 37, 1504-1514. (in Chinese) |
| [123] | Yin LJ (殷立娟), Wang P (王萍) (1997). Distribution of C3 and C4 photosynthetic pathways of plants on the steppe of Northeastern China. Acta Ecologica Sinica (生态学报), 17, 113-123. (in Chinese with English abstract) |
| [124] | Yun JY (云建英), Yang JD (杨甲定), Zhao HL (赵哈林) (2006). Research progress in the mechanism for drought and high temperature to affect plant photosynthesis. Acta Botanica Boreali-Occidentalia Sinica (西北植物学报), 26, 641-648. (in Chinese with English abstract) |
| [125] | Zhang JW (张经炜) (2006). C4 plants, one of the ways of desertification control. Arid Zone Research (干旱区研究), 23, 384-387. (in Chinese with English abstract) |
| [126] | Zhang X, Zwiers FW, Stott PA (2006). Multi-model multi-signal climate change detection at regional scale. Journal of Climate, 19, 4294-4307. |
| [127] | Zheng WJ, Zheng XP, Zhang CL (2000). A survey of photosynthetic carbon metabolism in 4 ecotypes of Phragmites australis in Northwest China: leaf anatomy, ultrastructure, and activities of ribulose 1,5-bisphosphate carboxylase, phosphoenolpyruvate carboxylase and glycollate oxidase. Physiologia Plantarum, 110, 201-208. |
| [128] | Zheng XP (郑学平), Zhang CL (张承烈), Chen GC (陈国仓) (1993). Investigation on the adaptation of photosynthetic carbon metabolism pathway to environment of Phragmites communis in Hexi Corridor of Gansu Province. Acta Phytoecologica et Geobotanica Sinica (植物生态学与地植物学学报), 17, 1-8. (in Chinese with English abstract) |
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