Abstract
Productivity of most improved major food crops showed stagnation in the past decades. As human population is projected to reach 9–10 billion by the end of the 21st century, agricultural productivity must be increased to ensure their demands. Photosynthetic capacity is the basic process underlying primary biological productivity in green plants and enhancing it might lead to increasing potential of the crop yields. Several approaches may improve the photosynthetic capacity, including integrated systems management, in order to close wide gaps between actual farmer’s and the optimum obtainable yield. Conventional and molecular genetic improvement to increase leaf net photosynthesis (P N) are viable approaches, which have been recently shown in few crops. Bioengineering the more efficient CC4 into C3 system is another ambitious approach that is currently being applied to the C3 rice crop. Two under-researched, yet old important crops native to the tropic Americas (i.e., the CC4 amaranths and the C3-CC4 intermediate cassava), have shown high potential P N, high productivity, high water use efficiency, and tolerance to heat and drought stresses. These physiological traits make them suitable for future agricultural systems, particularly in a globally warming climate. Work on crop canopy photosynthesis included that on flowering genes, which control formation and decline of the canopy photosynthetic activity, have contributed to the climate change research effort. The plant breeders need to select for higher P N to enhance the yield and crop tolerance to environmental stresses. The plant science instructors, and researchers, for various reasons, need to focus more on tropical species and to use the research, highlighted here, as an example of how to increase their yields.
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Abbreviations
- APAR:
-
absorbed photosynthetically active radiation
- C a :
-
ambient CO2 concentration
- C i :
-
intercellular CO2 concentration
- CA:
-
carbonic anhydrase
- g s :
-
stomatal conductance
- GDC:
-
glycine decarboxylase
- IRGA:
-
infra-red gas analyser
- LAI:
-
leaf area/land surface area index
- Km :
-
Michaelis constant
- NAD-ME:
-
NAD-malic enzyme
- NADP-ME:
-
NADP-malic enzyme
- P N :
-
net photosynthetic rate
- PEP:
-
phosphoenolpyruvate
- PEPC:
-
phosphoenolpyruvate carboxylase
- PEPCK:
-
PEP-carboxykinase
- PER:
-
protein efficiency ratio
- PNUE:
-
photosynthetic nitrogen-use efficiency
- PPDK:
-
pyruvate, phosphate dikinase
- RUE:
-
radiation-use efficiency
- TCA:
-
tricarboxylic acid
- Vmax :
-
maximum carboxylation rate
References
Affholder F., Poeydebat C., Corbeels M. et al.: The yield gap of major food crops in family agriculture in the tropics: assessment and analysis through field surveys and modelling. — Field Crop. Res. 143: 106–118, 2013.
Aguilar L.P.: [Leaf ultrastructure and photosynthesis in different cassava (Manihot esculenta Crantz) cultivars].–BSc. Thesis. Universidad del Cauca, Popayan 1995. [In Spanish]
Allem A.C.: The origin and taxonomy of cassava. — In: Hillocks R. J., Thresh J. M., Bellotti A. C. (ed.): Cassava: Biology, Production and Utilization. Pp. 1–16. CABI Publishing, New York 2002.
Amthor J.S.: From sunlight to phytomass: on the potential efficiency of converting solar radiation to phyto-energy. — New Phytol. 188: 939–959, 2010.
Angelov M.N., Sun J., Byrd G.T. et al.: Novel characteristics of cassava, Manhito esculenta Crantz, a reputed C3-C4 intermediate photosynthesis species. — Photsynth. Res. 38: 61–72, 1993.
Bhatt J.G., Rao M.R.K.: Heterosis in growth and photosynthetic rate in hybrids of cotton. — Euphytica 30: 129–133, 1981.
Baker J.M.: “It’s good for many things”: Wixárika (Huichol) ethnoecology of amaranth. — MSc. Thesis. University of Alberta, Edmonton 2006.
Bauwe H.: Photosynthetic enzyme activities in C3 and C3-C4 intermediate species of Moricandia and in Panicum millioides. — Photosynthetica 18: 201–209, 1984.
Bauwe H.: Photorespiration: the bridge to C4 photosynthesis. — In: Raghavendra A.S., Sage R.F. (ed.): C4 photosynthesis and related CO2 concentrating mechanisms. Pp. 81–108. Springer, Dordrecht 2011.
Berry J.A.: There ought to be an equation for that. — Annu. Rev. Plant Biol. 63: 1–17, 2012.
Berry J.O., McCormac D.J., Long J.J. et al.: Photosynthetic gene expression in amaranth, an NAD-ME type C4 dicot. — Aust. J. Plant Physiol. 24: 423–428, 1997.
Björkman O., Gauhl E., Nobs M.A.: Comparative studies of Atriplex species with and without β-carboxylation photosynthesis. — Carnegie Inst. Washington Yearbook 68: 620–633, 1969.
Björkman O., Nobs M., Pearcy R. et al.: Characteristics of hybrids between C3 and C4 species of Atriplex. — In: Hatch M.D., Osmond C.B., Slatyer R.O. (ed.): Photosynthesis and Photorespiration. Pp. 105–119. Wiley-Intersci. Publ., New York 1971.
Boardman N.K.: Comparative photosynthesis of sun and shade plants. — Annu. Rev. Plant Physio. 28: 355–377, 1977.
Borrell A., Hammer G., van Oosterom E.: Stay-green: A consequence of the balance between supply and demand for nitrogen during grain filling? — Ann. Bot.-London 138: 91–95, 2001.
Bowes G., Ogren W.L., Hageman R.H.: Phosphoglycolate production catalyzed by ribulose diphosphate carboxylase. — Biochem. Biophys. Res. Comun. 45: 716–722, 1971.
Briggs L.J., Shantz H.L.: Relative water requirement of plants. — J. Agr. Res. 3: 1–63, 1914.
Brownell P.F., Crossland C.J.: The requirement for sodium as a micronutrient by species having C4 dicarboxylic photo-synthetic pathway. — Plant Physiol. 49: 794–797, 1972.
Brown R.H.: A difference in the N use efficiency in C3 and C4 plants and its implications in adaptation and evolution. — Crop Sci. 18: 93–98, 1978.
Brown R.H., Byrd G.T., Bouton J.H., Bassett C.L: Photosynthetic characteristics of segregates from hybrids between Flaveria brownii (C4 like) and Flaveria linearis (C3-C4). — Plant Physiol. 101: 825–831, 1993.
Burnell J.N., Hatch M.D.: Low bundle sheath carbonic anhydrase is apparently essential for effective C4 pathway operation. — Plant Physiol. 86: 1252–1256, 1988.
Burnside C.A., Böhning R.H.: The effect of prolonged shading on the light saturation curves of apparent photosynthesis in sun plants. — Plant Physiol. 32: 61–63, 1957.
Busch F.A., Sage T.L., Cousins A.B., Sage R.F.: C3 plants enhance rate of photosynthesis by reassimilating photorespired and respired CO2. — Plant Cell Environ. 36: 200–212, 2013.
Calatayud P.A., Barón C.H., Velásquez J.A. et al.: Wild Manihot species do not possess C4 photosynthesis. — Ann. Bot. 89: 125–127, 2002.
Castrillo M., Aso P., Longart M., Vermehren A.: In situ immunofluorescent localization of ribulose-1,5-bisphosphate carboxylase/oxygenase in mesophyll of C4 dicotyledonous plants. — Photosynthetica 33: 39–50, 1997.
Cheng S.H., Cao L.Y., Yang S.H., Zhai H.Q.: Forty years’ development of hybrid rice: China’s experience. — Rice Sci. 11: 225–230, 2004.
Cheng S.H., Zhuang J.Y., Fan Y.Y. et al.: Progress in research and development on hybrid rice: A super-domesticate in China. — Ann. Bot.-London 100: 959–966, 2007.
Cock J.H., Franklin D., Sandoval G., Juri P.: The ideal cassava plant for maximum yield. — Crop Sci. 19: 271–279, 1979.
Cock J.H., Riaño N.M., El-Sharkawy M.A. et al.: C3-C4 intermediate photosynthetic characteristics of cassava (Manihot esculenta Crantz). II. Initial products of 14CO2 fixation. — Photosynth. Res. 12: 237–241, 1987.
Cock J.H., El-Sharkawy M.A.: Physiological characteristics for cassava selection. — Exp. Agri. 24: 443–448, 1988.
Connor D.J., Loomis R.S., Cassman K.G.: Crop Ecology: Productivity and Management in Agricultural Systems 2nd Ed. Pp. 562. Cambridge University Press, Cambridge 2011.
Connor J.K., Gartner R.J.W., Runge B.M., Amos R.N.: Amaranthus edulis: an ancient food source re-examined. — Aust. J. Exp. Agr. 20: 156–161, 1980.
Davis L.C.: Limiting factors in nitrogen fixation. — What’s New in Plant Physiology 11: 41–44, 1980.
de Tafur S.M., El-Sharkawy M.A., Calle F.: Photosynthesis and yield performance of cassava in seasonally dry and semiarid environments. — Photosynthetica 33: 249–257, 1997
Döring F., Streubel M., Bräutigam A., Gowik U.: Most photorespiratory genes are preferentially expressed in the bundle sheath cells of the C4 grass Sorghum bicolor. — J. Exp. Bot. March 14, 2016. doi: 10.1093/jxb/erw041.
Downton W.J.S.: Amaranthus edulis: a high lysine grain amaranth. — World Crop. 25: 20, 1973.
Duvall M.R., Saar D.E., Grayburn W.S., Holbrook G.P.: Complex transitions between C3 and C4 photosynthesis during the evolution of Paniceae: a phylogenetic case study emphasizing the position of Steinchisma hians (Poaceae), a C3-C4 intermediate. — Int. J. Plant Sci. 164: 949–958, 2003.
Edwards G.E., Sheta E., Moore B. et al.: Photosynthetic characteristics of cassava (Manihot esculenta Crantz), a C3 species with chlorenchymatous bundle sheath cells. — Plant Cell Physiol. 31: 1199–1206, 1990.
Ehleringer J.: Ecophysiology of Amaranthus palmeri, a Sonoran desert summer annual. — Oecologia 57: 1071–12, 1983.
Elmore C.D., Paul R.N.: Composite list of C4 weeds. — Weed Sci. 31: 686–692, 1983.
El-Sharkawy M.A: Factors limiting photosynthetic rates of different plant species. — PhD. Thesis. The University of Arizona, Tucson 1965.
El-Sharkawy M.A.: Drought-tolerant cassava for Africa, Asia, and Latin America: breeding projects work to stabilize productivity without increasing pressure on limited natural resources. — BioScience 43: 441–451, 1993.
El-Sharkawy M.A.: Cassava biology and physiology. — Plant Mol. Biol. 53: 621–641, 2003.
El-Sharkawy M.A.: Cassava biology and physiology. — Plant Mol. Biol. 56: 481–501, 2004.
El-Sharkawy M.A.: How can calibrated research-based models be improved for use as a tool in identifying genes controlling crop tolerance to environmental stresses in the era of genomics — from an experimentalist’s perspective. — Photosynthetica 43: 161–176, 2005.
El-Sharkawy M.A.: International research on cassava photosynthesis, productivity, eco-physiology, and responses to environmental stresses in the tropics. — Photosynthetica 44: 481–512, 2006.
El-Sharkawy M.A.: Pioneering research on C4 photosynthesis: Implications for crop water relations and productivity in comparison to C3 cropping systems. — J. Food Agric. Environ. 7: 468–484, 2009a.
El-Sharkawy M.A.: Pioneering research on C4 leaf anatomical, physiological, and agronomic characteristics of tropical monocot and dicot plant species: Implications for crop water relations and productivity in comparison to C3 cropping systems. — Photosynthetica 47: 163–183, 2009b.
El-Sharkawy M.A.: Cassava: physiological mechanisms and plant traits underlying tolerance to prolonged drought and their application for breeding improved cultivars in the seasonally dry and semiarid tropics. — In: DaMatta F.M. (ed.): Ecophysiology of Tropical Tree Crops. Pp. 71–110. Nova Sci. Publ., New York 2010.
El-Sharkawy M.A.: Stress-tolerant cassava: the role of integrative ecophysiology-breeding research in crop improvement. — Open J. Soil Sci. 2: 162–186, 2012.
El-Sharkawy M.A.: Global warming: causes and impacts on agroecosystems productivity and food security with emphasis on cassava comparative advantage in the tropics/subtropics. — Photosynthetica 52: 161–178, 2014.
El-Sharkawy M.A., Cock J.H.: Water use efficiency of cassava. I. Effects of air humidity and water stress on stomatal conductance and gas exchange. — Crop Sci. 24: 497–502, 1984.
El-Sharkawy M.A., Cock J.H.: C3-C4 intermediate photosynthetic characteristics of cassava (Manihot esculenta Crantz).I. Gas exchange. — Phototsynth. Res. 12: 219–235, 1987a.
El-Sharkawy M.A., Cock J.H.: Response of cassava to water stress. — Plant Soil 100: 345–360, 1987b.
El-Sharkawy M.A., Cock J.H.: Photosynthesis of cassava (Manihot esculenta Crantz). — Exp. Agri. 26: 325–340, 1990.
El-Sharkawy M.A., de Tafur S.M.: Genotypic and within canopy variation in leaf carbon isotope discrimination and its relation to short-term leaf gas exchange characteristics in cassava grown under rain-fed conditions in the tropics. — Photosynthetica 45: 515–526, 2007.
El-Sharkawy M.A., de Tafur S.M.: Comparative photosynthesis, growth, productivity, and nutrient use efficiency among talland short-stemmed rain-fed cassava cultivars. — Photosynthetica 48: 173–188, 2010.
El-Sharkawy M.A., Hesketh J.D.: Effects of temperature and water deficit on leaf photosynthetic rates of different species. — Crop Sci. 4: 514–518, 1964.
El-Sharkawy M., Hesketh J.: Photosynthesis among species in relation to characteristics of leaf anatomy and CO2 diffusion resistances. — Crop Sci. 5: 517–521, 1965.
El-Sharkawy M.A., Hesketh J.D.: Citation Classic-Photosynthesis among species in relation to characteristics of leaf anatomy and CO2 diffusion resistances. — Curr. Cont. /Agr. Biol. Environ. 27: 14, 1986.
El-Sharkawy M.A., Cock J.H., de Cadena G.: Influence of differences of leaf anatomy on net photosynthetic rates of some cultivars of cassava. — Photosynth. Res. 5: 235–242, 1984a.
El-Sharkawy M.A., Cock J.H., de Cadena G.: Stomatal characteristics among cassava cultivars and their relation to gas exchange. — Exp. Agri. 20: 67–76, 1984b.
El-Sharkawy M.A., Cock J.H., Held A.A.: Photosynthetic responses of cassava cultivars (Manihot esculenta Crantz) from different habitats to temperature. — Photosynth. Res. 5: 243–250, 1984c.
El-Sharkawy M.A., Cock J.H., Held A.A.: Water use efficiency of cassava. II: Differing sensitivity of stomata to air humidity in cassava and other warm climate species. — Crop Sci. 24: 503–507, 1984d.
El-Sharkawy M.A., Cock J.H., Hernandez A.D.P.: Stomatal response to air humidity and its relation to stomatal density in a wide range of warm climate species. — Photosynth. Res. 7: 137–149, 1985.
El-Sharkawy M.A., de Tafur S.M., Cadavid L.F.: Potential photosynthesis of cassava as affected by growth conditions. — Crop Sci. 32: 1336–1342, 1992a.
El-Sharkawy M.A., de Tafur S.M., Cadavid L.F.: Photosynthesis of cassava and its relation to crop productivity. — Photosynthetica 28: 431–438, 1993.
El-Sharkawy M.A., de Tafur S.M., Lopez Y.: Cassava productivity, photosynthesis, ecophysiology, and response to environmental stresses in the tropics: a multidisciplinary approach to crop improvement and sustainable production. — In: Ospina B., Ceballos H. (ed.): Cassava in the Third Millennium: Modern Production, Processing, Use, and Marketing Systems. Pp. 29–88. CIAT, Cali 2012a.
El-Sharkawy M.A., de Tafur S.M., Lopez Y.: Integrative ecophysiological research for breeding improved cassava cultivars in favorable and stressful environments in the tropical/subtropical bio-systems. — In: Gorawala P., Mandhatri S. (ed.): Agricultural Research Updates, Vol. 4. Pp. 1–76. Nova Sci. Publ., New York 2012b.
El-Sharkawy M.A., Hernández A.D.P., Hershey C.: Yield stability of cassava during prolonged mid-season water stress. — Exp. Agr. 28: 165–174, 1992b.
El-Sharkawy M.A., Hesketh J., Muramoto H.: Leaf photosynthetic rates and other growth characteristics among 26 species of Gossypium. — Crop Sci. 5: 173–175, 1965.
El-Sharkawy M.A., Loomis R.S., Williams W.A.: Apparent reassimilation of respiratory carbon dioxide by different plant species. — Physiol. Plantarum 20: 171–186, 1967.
El-Sharkawy M.A., Loomis R.S., Williams W.A.: Photosynthetic and respiratory exchanges of carbon dioxide by leaves of grain amaranth. — J. Appl. Ecol. 5: 243–251, 1968.
El-Sharkawy M.A., Lopez Y., Bernal L.M.: Genotypic variations in activities of phosphoenolpyruvate carboxylase (PEPC) and correlations with leaf photosynthetic characteristics and crop productivity of cassava grown in lowland seasonally dry tropics. — Photosynthetica 46: 238–247, 2008.
El-Sharkawy M.A., Cock J.H., Lynam J.K. et al.: Relationships between biomass, root-yield and single-leaf photosynthesis in field-grown cassava. — Field Crop. Res. 25: 183–201, 1990.
Evans L.T.: Crop Evolution, Adaptation and Yield. Pp. 500. Cambridge University Press, Cambridge 1993.
Everson R.G., Slack. C.R.: Distribution of carbonic anhydrase in relation to the C4 pathway of photosynthesis. — Phytochemistry 7: 581–584, 1968.
FAO: Adaptation to climate change in agriculture, forestry and fisheries: perspective, framework and priorities. Pp. 24. FAO, Rome 2007.
Fedoroff N.V.: McClintock’s challenge in the 21st century. — P. Natl. Acad. Sci. USA 109: 20200–20203, 2012.
Fischer R.A., Byerlee D., Edmeades G.O.: Crop Yields and Global Food Security: will Yield Increase Continue to Feed the World?. Pp. 634. Austr. Centre Int. Agr. Res., Canberra 2014.
Fischer R.A., Rees D., Sayre K.D et al.: Wheat yield progress is associated with higher stomatal conductance, higher photosynthetic rate and cooler canopies. — Crop Sci. 38: 1467–1475, 1998.
Fisher A.E., McDade L.A., Kiel C.A. et al: Evolutionary history of Blepharis (Acanthaceae) and the origin of C4 photosynthesis in section Acanthodium. — Int. J. Plant Sci. 176: 770–790, 2015.
George T.S., Hawes C., Newton A.C. et al.: Field phenotyping and long-term platforms to characterise how crop genotypes interact with soil processes and the environment.–Agronomy 4: 242–278, 2014.
Gibbons A.: New view of early Amazonia. — Science 248: 1488–1490, 1990.
Gilmanov T.G., Baker J.M., Bernachii C.J. et al.: Productivity and carbon dioxide exchange of leguminous crops: estimates from flux towers measurements. — Agron. J. 106: 545–559, 2014.
Gowik U., Westhoff P.: The path from C3 to C4 photosynthesis. — Plant Physiol. 155: 56–63, 2011.
Gready J.E., Dwyer S.A., Evans J.R. (ed.).: Applying Photosynthesis Research to Improvement of Food Crops. Proceedings of a Workshop Held at the Australian National University, Canberra, ACT, Australia, 2–4 September 2009. Pp. 145. ACIAR Proceedings 140. Austr. Centre Int. Agr. Res., Canberra 2013.
Hand D.W., Warren Wilson J., Acock B.: Effects of light and CO2 on net photosynthetic rates of stands of aubergine and Amaranthus. — Ann. Bot.-London 71: 209–216, 1993.
Hatch M.D., Burnell J.M.: Carbonic anhydrase activity in leaves and its role in the first step of C4 photosynthesis. — Plant Physiol. 93: 825–828, 1990.
Hatch M.D., Slack C.R.: Photosynthetic CO2-fixation pathways. — Annu. Rev. Plant Physio. 21: 141–162, 1970.
Hatch M.D., Slack C.R., Johnson H.S.: Further studies on a new pathway of photosynthetic CO2 fixation in sugar cane and its occurrence in other plant species. — Biochem. J. 102: 417–422, 1967.
Hatfield J.L., Walthall C.L.: Meeting global food needs: realizing the potential via genetics x environment x management interactions. — Agron. J. 107: 1215–1226, 2015.
Hauptli H., Jain S.K.: Biosystematics and agronomic potential of some weedy and cultivated amaranths. — Theor. Appl. Genet. 52: 177–185, 1978.
Hershey C.H., Jennings D.L.: Progress in breeding cassava for adaptation to stress. — Plant Breed. Abstr. 62: 823–831, 1992.
Hesketh J., Muramoto H., El-Sharkawy M.: Carbonic Anhydrase and Photosynthesis in Leaves among Species. Rep. no. 2 on Photosynthesis. Pp. 15. Dept. Plant Breeding, Univ. Arizona, Tucson 1965.
Hong J., Jiang D.-A, Weng X.-Y et al.: Leaf anatomy,chloroplast ultrastructure, and cellular localization of ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBPCO) and RuBPCO activase in Amaranthus tricolor L. — Photosynthetica 43: 519–528, 2005.
Holaday A.S., Chollet R.: Photosynthetic/photorespiratory characteristics of C3-C4 intermediate species. — Photosynth. Res. 5: 307–323, 1984.
Holaday A.S., Brown R.H., Bartlett J.M. et al.: Enzymic and photosynthetic characteristics of reciprocal F1 hybrids of Flaveria pringlei (C3) and Flaveria brownii (C4-like species). — Plant Physiol. 87: 484–490, 1988.
Houghton R.A.: Carbon. — In: Turner B.L., Clark W.C., Kates R.W. et al. (ed.).: The Earth as Transformed by Human Action. Pp. 393–408. Cambridge University Press, Cambridge 1990.
Huang X., Yang S., Gong J. et al.: Genomic analysis of hybrid rice varieties reveals numerous superior alleles that contribute to heterosis. — Nat. Commun. 6: 6258, 2015.
Hylton C.M., Rawsthorne S., Smith A.M. et al.: Glycine decarboxylase is confined to the bundle-sheath cells of leaves of C3-C4 intermediate species. — Planta. 175: 452–459, 1988.
Igamberdiev A.U., Roussel M.R.: Feedforward non-Michaelis-Menten mechanism for CO2 uptake by Rubisco: contribution of carbonic anhydrases and photorespiration to optimization of photosynthetic carbon assimilation. — Biosystems 107: 158–166, 2012.
Igamberdiev A.U.: Control of Rubisco function via homeostatic equilibration of CO2 supply. — Front. Plant Sci. 6: 106, 2015.
Jackson W.A., Volk R.J.: Oxygen uptake by illuminated maize leaves. — Nature 222: 269–271, 1969.
Jackson W.A., Volk R.J.: Photorespiration. — Annu. Rev. Plant Physio. 21: 385–432, 1970.
Jarvis A., Ramirez-Villegas J., Herrera Campo J.B., Navarro-Racines C.: Is cassava the answer to African climate change adaptation? — Tropical Plant Biol. 5: 9–29, 2012.
Johnson B.L., Henderson T.L.: Water use patterns of grain amaranth in the northern great plains. — Agron. J. 94: 1437–1443, 2002.
Johnston M., Grof C.P.L., Brownell P.F.: Responses to ambient CO2 concentrations by sodium-deficient C4 plants. — Aust. J. Plant Physiol. 11: 137–141, 1984.
Kelly J.G., Latzko E.: Thirty Years of Photosynthesis. 1974 — 2004. Pp. 414. Springer, Berlin-Heidelberg-New York 2006.
Keerberg O., Pämik T., Ivanova H. et al.: C2 photosynthesis generates about 3-fold elevated leaf CO2 levels in the C3–C4 intermediate species Flaveria pubescens. — J. Exp. Bot. 65: 3649–3656, 2014.
Kering M.K.: Manganese nutrition and photosynthesis in NAD-malic enzyme C4 plants. — Ph.D. Thesis. The University of Missouri, Columbia 2008.
Kiirats O., Lea P.J., Franceschi V.R., Edwards G.E.: Bundle sheath diffusive resistance to CO2 and effectiveness of C4 photosynthesis and refixation of photorespired CO2 in C4 cycle mutant and wild-type Amaranthus edulis. — Plant Physiol. 130: 964–976, 2002.
Kiniry J.R., Jones C.A., O’Toole J.C. et al.: Radiation-use efficiency in biomass accumulation prior to grain-filling for five grain-crop species. — Field Crop. Res. 20: 51–64, 1989.
Kirkham M.B.: Elevated Carbon Dioxide: Impacts on Soil and Plant Water Relations. Pp. 399. CRC Press, Boca Raton 2011.
Kennedy R.A., Laetsch W.M.: Plant species intermediate for C3, C4 photosynthesis. — Science 184: 1087–1089, 1974.
Kozaki A., Takeba G.: Photorespiration protects C3 plants from photooxidation. — Nature 384: 557–560, 1996.
Laetsch W.M.: The C4 syndrome: a structural analysis. — Annu. Rev. Plant Physio. 25: 27–52, 1974.
Langdale J.A., Nelson T.: Spatial regulation of photosynthetic development. — Trends Genet. 7: 191–196, 1991.
Lehmann J.W: Hybridization and growth studies in the grain amaranths (Amaranthus hybridus L.). — Ph.D. Thesis. Iowa State University, Ames 1989.
Lenis J.I., Calle F., Jaramillo G. et al.: Leaf retention and cassava productivity. — Field Crop. Res. 95: 126–134, 2006.
Lester J.N., Goldsworthy A.: The occurrence of high CO2-compensation points in Amaranthus species. — J. Exp. Bot. 24: 1031–1034, 1973.
Lin Z.F., Ehleringer J.: Photosynthetic characteristics of Amaranthus tricolor, a C4 tropical leafy vegetable. — Photosynth. Res. 4: 171–178, 1983.
Lindquist J.L., Arkebauer T.J., Walters D.T. et al.: Maize radiation use efficiency under optimal growth conditions. — Agron. J. 97: 72–78, 2005.
Liu Y., Wu L., Baddeley J.A. Watson C.A.: Models of biological nitrogen fixation of legumes. A review. — Agron. Sustain. Dev. 31: 155–172, 2011.
Lobell D.B., Cassman K.G., Field C.B.: Crop Yield Gaps: Their Importance, Magnitudes, and Causes. — Annu. Rev. Env. Resour. 34: 179–204, 2009
Loomis R.S., Amthor J.S.: Yield potential, plant assimilatory capacity, and metabolic efficiencies. — Crop Sci. 39: 1584–1596, 1999.
Long S.P., Ainsworth E.A., Leakey A.D.B. et al.: Food for thought: lower-than-expected crop yield stimulation with rising CO2 concentration. — Science 312: 1918–1921, 2006.
Lundgren M.R., Osborne C.P., Christin P.-A.: Deconstructing Kranz anatomy to understand C4 evolution. — J. Exp. Bot. 65: 3357–3369, 2014.
Lutz W., Butz W.P., Samir K.C. (ed.): World Population and Human Capital in the Twenty-First Century. Pp. 1072. Oxford Univ. Press, Oxford 2014.
Lynch J.P.: Root phenes that reduce the metabolic costs of soil exploration: opportunities for 21st century agriculture. — Plant Cell Environ. 38: 1775–1784, 2015.
Magnin N.C., Cooley B.A., Reiskind J.B., Bowes G.: Regulation and localization of key enzymes during the induction of Kranzless, C4–type photosynthesis in Hydrilla verticillata. — Plant Physiol. 115: 1681–1689, 1997.
Milthorpe F.L. (ed.).: The Growth of Leaves. Pp. 223. Butterworth’s Sci. Publ., London. 1956.
Monson R.K.: On the evolutionary pathways resulting in C4 photosynthesis and crassulacean acid metabolism (CAM). — Adv. Ecol. Res. 19: 57–110, 1989.
Monson R.K., Rawsthorne S.: Carbon dioxide assimilation in C3–C4 intermediate plants. — In: Leegood R.C., Sharkey T.D., von Caemmerer S.(ed.): Photosynthesis: Physiology and Metabolism. Pp. 533–550. Kluwer Academic Press, Dordrecht 2000.
Monson R.K., Edwards G.E., Ku M.S.B.: C3-C4 intermediate photosynthesis in plants. — BioScience 34: 563–574, 1984.
Muramoto H., Hesketh J., El-Sharkawy M.A.: Relationships among rate of leaf area development, photosynthetic rate, and rate of dry matter production among American cultivated cottons and other species. — Crop Sci. 5: 163–166, 1965.
Nasyrov Y.S.: Genetic control of photosynthesis and improving of crop productivity. — Annu. Rev. Plant Physio. 29: 215–237, 1978.
Nasyrov Y.S.: Genetic modification of the CO2 carboxylation reactions as a factor improving efficiency of photosynthesis. — Indian J. Plant Physiol. 24: 26–36, 1981.
Nelson T., Langdale J.A.: Pattern of leaf development in C4 plants. — Plant Cell 1: 3–13, 1989.
Nelson T., Langdale J.A.: Developmental genetics of C4 photosynthesis. — Annu. Rev. Plant Phys. 43: 25–47, 1992.
NRC (National Research Council).: Amaranthus: Modern Prospects for an Ancient Crop. Pp. 80. Nat. Acad. Press, Wahington, D.C. 1984.
NRC (National Research Council).: Lost Crops of the Incas: Little-Known Plants of the Andes with Promise for Worldwide Cultivation. Pp. 415. Nat. Acad. Press, Washington, D.C. 1989.
Oakley J.C., Sultmanis S., Stinson C.R. et al.: Comparative studies of C3 and C4 Atriplex hybrids in the genomics era: physiological assessments. — J. Exp. Bot. 65: 3637–3647, 2014.
Oaks A.: Efficiency of nitrogen utilization in C3 and C4 cereals. — Plant Physiol. 106: 407–414, 1994.
Ogren W.L.: Photorespiration: pathways, regulation, and modification. — Annu. Rev. Plant Physio. 35: 415–442, 1984.
Parry M.A.J., Reynolds M.P., Salvucci M.E. et al.: Raising yield potential of wheat. II. Increasing photosynthetic capacity and efficiency. — J. Exp. Bot. 62: 453–467, 2011.
Pearcy R.W., Ehleringer J.: Comparative ecophysiology of C3 and C4 plants. — Plant Cell Environ. 7: 1–13, 1984.
Pellet D., El-Sharkawy M.A.: Cassava response to phosphorus fertilization. I. Yield, biomass and gas exchange. — Field Crop. Res. 35: 1–11, 1993.
Pellet D., El-Sharkawy M. A.: Sink Source relations in cassava: effects of reciprocal grafting on yield and leaf photosynthesis. — Exp. Agri. 30: 359–367, 1994.
Peng S., Huang J., Sheehy J.E. et al.: Rice yields decline with higher night temperature from global warming. — P. Natl. Acad. Sci. USA 101: 9971–9975, 2004.
Penning de Vries F.W.T., Jansen D.M., ten Berge H.FM., Bakema A.: Simulation of Ecophysiological Processes of Growth in Several Annual Crops. Pp. 271. PUDOC, Wangeningen 1989.
Phillips D.A.: Efficiency of symbiotic nitrogen fixation in legumes. — Annu. Rev. Plant Physio. 31: 29–49, 1980.
Poorter H., Niinemets Ü., Poorter L. et al.: Causes and consequences of variation in leaf mass per area (LMA): a metaanalysis. — New Phytol. 182: 565–588, 2009.
Porter J.R., Xie L., Challinor A.J. et al.: IPCC: Food Security and Food Production Systems (WG II AR5), Chap. 7. Climate Change 2014: Impacts, Adaptation, and Vulnerability. Pp. 485–533. Cambridge and New York 2014.
Porto M.C.M.: Physiological mechanisms of drought tolerance in cassava (Manihot esculenta Crantz). — PhD. Thesis. The University of Arizona, Tucson 1983.
Rabbi I., Hamblin M., Gedil M. et al.: Genetic mapping using genotyping-by-sequencing in the clonally propagated cassava. — Crop Sci. 54: 1–13, 2014.
Rawsthorne S.: C3-C4 intermediate photosynthesis: linking physiology to gene expression. — Plant J. 2: 267–274, 1992.
Ray D.K., Mueller N.D., West P.C., Foley J.A.: Yield trends are insufficient to double global food production by 2050.— PloS One 8: e66428, 2013.
Reiskind J.B., Madsen T.V., Van Ginkel L.C., Bowes G.: Evidence that inducible C4-type photosynthesis is a chloroplastic CO2-concentrating mechanism in Hydrilla, a submersed monocot. — Plant Cell Environ. 20: 211–220, 1997.
Renvoize B.S.: The area of origin of Manihot esculenta. — Econ. Bot. 26: 352–360, 1972.
Reynolds M., Foulkes J., Furbank R. et al.: Achieving yield gains in wheat. — Plant Cell Environ. 35: 1799–1823, 2012.
Riaño N.M., Cock J.H., Lopez F.Y., El-Sharkawy M A.: [Kranz anatomy, structure, and distribution of chloroplasts in cassava (Manihot esculenta Crantz) leaves]. — Revista Comalfi 14: 5–12, 1987a. [In Spanish]
Riaño M.A., Cock J.H., López Y. et al.: [Photosynthetic characteristics of cassava (Manihot esculenta Crantz): initial products of 14CO2 fixation]. — Revista Comalfi 14: 13–17, 1987b. [In Spanish]
Rosenthal D., Ort D.R.: Examining cassava’s potential to enhance food security under climate change. — Trop. Plant Biol. 5: 30–38, 2012.
Rylott E.L., Metzlaff K., Rawsthorne S.: Developmental and environmental effects on the expression of the C3-C4 intermediate phenotypes in Moricandia arvensis. — Plant Physiol. 118: 1277–1284,1998.
Sage R.F.: The evolution of C4 photosynthesis. — New Phytol. 161: 341–370, 2004.
Sage R.F.: Photorespiratory compensation: a driver for biological diversity. — Plant Biol. 15: 624–638, 2013.
Sage R.F., Pearcy R.W.: The nitrogen use efficiency of C3 and C4 plants I. Leaf nitrogen, growth, and biomass partitioning in Chenopodium album (L.) and Amaranthus retroflexus (L.). — Plant Physiol. 84: 954–958, 1987.
Sage R.F., Seemann J.R.: Regulation of ribulose- 1,5-bisphosphate carboxylase/oxygenase activity in response to reduced light intensity in C4 plants. — Plant Physiol. 102: 21–28, 1993.
Sage R.F., Christin P.-A., Edwards E.K.: The C4 plant lineages of planet Earth. — J. Exp. Bot. 62: 3155–3169, 2011a.
Sage R.F., Sage T.L., Kocacinar F.: Photorespiration and the Evolution of C4 photosynthesis. — Annu. Rev. Plant Biol. 63: 19–47, 2012.
Sage R.F., Sage T.L., Pearcy R.W., Borsch T.: The taxonomic distribution of C4 photosynthesis in Amaranthaceae sensu stricto. — Am. J. Bot. 94: 1992–2003, 2007.
Sage T.L., Busch F.A., Johnson D.C. et al: Initial events during the evolution of C4 photosynthesis in C3 species of Flaveria. — Plant Physiol. 163: 1266–1276, 2013.
Sage T.L., Sage R.F., Vogan P.J. et al.: The occurrence of C2 photosynthesis in Euphorbia subgenus Chamaesyce (Euphorbiaceae). — J. Exp. Bot. 62: 3183–3195, 2011b
Saithong T., Rongsirikul O., Kalapanulak S. et al.: Starch biosynthesis in cassava: a genome-based pathway reconstruction and its exploitation in data integration. — BMC Syst. Biol. 7: 75, 2013.
Sasson A.: Feeding Tomorrow’s World. Pp. 805. UNISCO/CTA, Paris 1990.
Sauer J.D.: The grain Amaranths: A Survey of their History and Classification. — Ann. Mo. Bot. Gard. 37: 561–632, 1950.
Sauer J.D: The Grain Amaranths and their Relatives: A Revised Taxonomic and Geographic Survey. — Ann. Mo. Bot. Gard. 54: 103–137, 1967.
Sawada S., Sakamoto T., Sato M. et al.: Photosynthesis with single-rooted Amaranthus leaves. II. Regulation of ribulose-1,5-bisphosphate carboxylase, phosphoenolpyruvate carboxylase, NAD-malic enzyme and NAD-malate dehydrogenase and coordination between PCR and C4 photosynthetic metabolism in response to changes in the source-sink balance. — Plant Cell Physiol. 43: 1293–1301, 2002.
Schonbeck M.: Weed Profile: Pigweeds (Amaranthus spp.). — eXtension, March 10, 2014. http://www.extension.org/pages/65208/weed-profile:-pigweeds-amaranthus-spp#.VhvG8_mqqkp
Shantz H.L., Piemeisel L.N.: The water requirements of plants at Akron, CO. — J. Agr. Res. 34: 1093–1190, 1927.
Sheehy J.E., Mitchell P.L., Hardy B. (ed.): Redesigning rice Photosynthesis to increase Yield. Proceedings of the Workshop on The Quest to Reduce Hunger: Redesigning Rice Photosynthesis, 30 Nov.-3 Dec. 1999. Los Baños, Philippines. Makati City (Philippines). Pp. 293. Elsevier Sci., Amsterdam 2000.
Sheehy J.E., Mitchel P.L., Hardy B. (ed.): Charting New Pathways to C4 Rice. Pp 422. Int. Rice Res. Inst. Los Baños 2007.
Sheen J.Y.: C4 gene expression. — Annu. Rev. Plant Phys. 50: 187–217, 1999.
Sinclair T.R., Horie T.: Leaf nitrogen, photosynthesis, and crop radiation use efficiency: A review. — Crop Sci. 29: 90–98, 1989.
Sinclair T.R., Muchow R.C.: Radiation use efficiency. — Adv. Agron. 65: 215–265, 1999.
Stoy V.: Interrelationships Among Photosynthesis, Respiration, and Movement of Carbon in Developing Crops. Pp. 24. Agr. & Hortic. Dep. Univ. Nebrasca, Lincoln 1969.
Tanz S.K., Tetu S.G., Vella N.G.F., Ludwig M.: Loss of the transit peptide and an increase in gene expression of an ancestral chloroplastic carbonic anhydrase were instrumental in the evolution of the cytosolic C4 carbonic anhydrase in Flaveria. — Plant Physiol. 150: 1515–1529, 2009.
Tazoe Y., Noguchi K.O., Terashima I.: Effects of growth light and nitrogen nutrition on the organization of the photosynthetic apparatus in leaves of a C4 plant, Amaranthus cruentus. — Plant Cell Environ. 29: 691–700, 2006.
Tittonell P., Giller K.E.: When yield gaps are poverty traps: The paradigm of ecological intensification in African smallholder agriculture. — Field Crop. Res. 143: 76–90, 2013.
Tolbert N.E.: Microbodies-peroxisomes and glyoxysomes. — Annu. Rev. Plant Physio. 22: 45–74, 1971.
Tolbert N.E., Oeser A., Yamazaki R.K. et al.: A survey of plants for peroxisomes. — Plant Physiol. 44: 135–147, 1969.
Triolo L., Bagnara D., Anselmi L., Bassanelli C.: Carbonic anhydrase activity and localization in some plant species. — Physiol. Plantarum 31: 86–89, 1974.
Tubiello F.N., Soussana J-F., Howden S.M.: Crop and pasture response to climate Change. — P. Natl. Acad. Sci. USA 104: 19686–19690. 2007.
Tucker J.B.: Amaranth: the once and future crop. — BioScience 36: 9–13, 1986.
Ueno O.: Immunocytochemical localization of enzymes involved in the C3 and C4 pathways in the photosynthetic cells of an amphibious sedge, Eleocharis vivipara. — Planta 199: 394–403, 1996.
Ueno O.: Environmental regulation of C3 and C4 differentiation in the amphibious sedge, Eleocharis vivipara. — Plant Physiol. 127: 1524–1532, 2001.
Ueno O., Agarie S.: The intercellular distribution of glycine decarboxylase in leaves of cassava in relation to the photosynthetic mode and leaf anatomy. — Jap. J. Crop Sci. 66: 268–278, 1997.
Ugent D., Pozorski S., Pozorski T.: Archaeological manioc (Manihot) from coastal Peru. — Econ. Bot. 40: 78–102, 1986.
van Ittersum M.K., Cassman K.G., Grassini P. et al.: Yield gap analysis with local to global relevance — A review. — Field Crop. Res. 143: 4–17, 2013.
Vance C.P., Heichel G.H.: Carbon in N2 fixation: limitation or exquisite adaptation. — Annu. Rev. Plant Phys. 42: 373–390, 1991.
Veltkamp H.J.: Physiological causes of yield variation in cassava (Manihot esculenta Crantz). — PhD. Thesis, Wageningen Agricultural University, Wageningen 1986.
Volk R.J., Jackson W.A.: Photorespiratory phenomena in maize. — Plant Physiol. 49: 218–223, 1972.
von Caemmerer S., Furbank R.T. (ed.): C4 photosynthesis: 30 (or 40) years on. — Aust. J. Plant Physiol. 24: 409–555, 1997.
Voznesenskaya E.V., Franceschi V.R., Kiirats O. et al.: Proof of C4 photosynthesis without Kranz anatomy in Bienertia cycloptera (Chenopodiaceae). — Plant J. 31: 649–662, 2002.
Voznesenskaya E.V., Franceschi V.R., Kiirats O. et al.: Kranz anatomy is not essential for terrestrial C4 plant photosynthesis. — Nature 414: 543–546, 2001.
Voznesenskaya E.V., Koteyeva1 N.K., Edwards G.E., Ocampo G.: Revealing diversity in structural and biochemical forms of C4 photosynthesis and a C3–C4 intermediate in genus Portulaca L. (Portulacaceae). — J. Exp. Bot. 61: 3647–3662, 2010.
Wang J.L., Klessig D.F., Berry J.O.: Regulation of C4 gene expression in developing Amaranth leaves. — Plant Cell 4: 173–184, 1992.
Webster T.M.: Weed survey — southern states. Vegetable, fruit and nut crops subsection. — Proc. South. Weed Sci. Soc. 59: 260–277, 2006.
Westhoff P., Gowik U.: Evolution of C4 phosphoenolpyruvate carboxylase-genes and proteins: a case study with the genus Flaveria. — Ann. Bot.-London 93: 13–23, 2004.
Whitehead W.F., Carter J., Singh B.P.: Effect of planting date on vegetable amaranth leaf yield, plant height, and gas exchange. — HortScience 37: 773–777, 2002.
Wu X-Y., Gu W., Wu G.-Y.: Rubisco from Amaranthus hypochondriacus. — In: Baltscheffsky M. (ed.): Current Research in Photosynthesis, vol. III. Pp. 339–342. Kluwer Academic Publishers, Dordrecht 1990.
Yin X., Struik P.C.: Constraints to the potential efficiency of converting solar radiation into phytoenergy in annual crops: from leaf biochemistry to canopy physiology and crop ecology. — J. Exp. Bot. 66: 6535–6549, 2015
Zahran H.H.: Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. — Microbiol. Mol. Biol. Rev. 63: 968–989,1999.
Zelitch I.: The close relationship between net photosynthesis and crop yield. — BioScience 32: 796–802, 1982.
Zhu X.-G., Long S.P., Ort D.R.: Improving photosynthetic efficiency for greater yield. — Annu. Rev. Plant Biol. 61: 235–261, 2010.
Ziska L.H., Dukes J.F. (ed.): Invasive Species and Global Climate Change. Pp 368. CABI, Wallingford 2014.
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Acknowledgements: I am grateful to the Photosynthetica’s invitation to write this review, and to the Natives of the Americas, who provided us with the opportunity to research, and rediscover the high photosynthetic capacities of the C4 amaranths, and the C3-C4 intermediate cassava. Invaluable comments by M.B. Kirkham, A.U Igamberdiev, J.D. Hesketh, and from Photosynthetica reviewers and editors were included in the final version. The many articles reprints received from R.F. Sage and J.P. Lynch were appreciated. Thanks to S.M. de Tafur, S. Navarro de El-Sharkawy, and F. El-Sharkawy Navarro, for their needed support and assistance.
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El-Sharkawy, M.A. Prospects of photosynthetic research for increasing agricultural productivity, with emphasis on the tropical C4 Amaranthus and the cassava C3-C4 crops. Photosynthetica 54, 161–184 (2016). https://doi.org/10.1007/s11099-016-0204-z
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DOI: https://doi.org/10.1007/s11099-016-0204-z