Abstract
Early in his career, Russ Monson produced a series of influential eco-physiological papers that helped lay the foundation for the study of C4 plant evolution. Among the most important was a 1984 paper with Maurice Ku and Gerry Edwards that outlined the pathway for the evolutionary bridge from C3 to C4 photosynthesis. This model proposed C4 photosynthesis arose out of a shuttle that imported photorespiratory metabolites into bundle sheath (BS) cells, where glycine decarboxylase cleaved off CO2, allowing it to accumulate and be efficiently refixed by BS Rubisco. By the mid-1990’s, Monson’s research focus had shifted away from C4 plants, save for one 2003 paper on C3 versus C4 stomatal control with Travis Huxman, and a series of critical reviews on C4 evolution. These reviews heavily influenced the modern synthesis of C4 evolutionary studies, which incorporates phylogenomic understanding with physiological, molecular, and structural characterizations of trait shifts in multiple evolutionary lineages. Subsequent research supported the Monson et al. model from 1984, by showing a glycine shuttle occurs in nearly all C3–C4 intermediate species identified. Monson also examined the physiological controls over the ecological distribution of C3, C3–C4 intermediate, and C4 photosynthesis, building our understanding of the fitness value of the intermediate and C4 pathway in relevant microenvironments. By establishing the foundation for discoveries that followed, Russ Monson can rightly be considered a leading pioneer contributing to the evolutionary biology of C4 photosynthesis.
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References
Alonso-Cantabrana H, von Caemmerer S (2016) Carbon isotope discrimination as a diagnostic tool for C4 photosynthesis in C3–C4 intermediate species. J Exp Bot 67:3109–3121. https://doi.org/10.1093/jxb/erv555
Apel P, Maass I (1981) Photosynthesis in species of Flaveria: CO2 compensation concentration, O2 influence on photosynthetic gas exchange and δ13C values in species of Flaveria (Asteraceae). Biochemie und Physiologie der Pflanzen 176:396–399. https://doi.org/10.1016/S0015-3796(81)80052-2
Apel P, Ohle H (1979) CO2-Kompensationpunkt und Blattenanatomie bei Arten der Gattung Moricandia DC. (Brassicaceae). Biochem Physiol Pflanzen 174:68–75
Bauwe H (2011) Photorespiration: the bridge to C4 photosynthesis. In: Raghavendra AS, Sage RF (eds) C4 photosynthesis and related CO2 concentrating mechanisms. Springer, Dordrecht, pp 81–108
Bjorkman O (1976) Adaptive and genetic aspects of C4 photosynthesis. In: Burris RH, Black CC (eds) CO2 metabolism and plant productivity. University Park Press, Baltimore, pp 287–309
Black CC (1971) Ecological implications of dividing plants into groups with distinct photosynthetic production capacities. Adv Ecol Res 7:87–114
Bohley K, Schröder T, Kesselmeier J et al (2019) C4-like photosynthesis and the effects of leaf senescence on C4-like physiology in Sesuvium sesuvioides (Aizoaceae). J Exp Bot 70:1553–1565. https://doi.org/10.1093/jxb/erz011
Bolton JK, Brown RH (1980) Photosynthesis of grass species differing in carbon dioxide fixation pathways: V. response of Panicum maximum, Panicum milioides, and tall fescue (Festuca arundinacea) to nitrogen nutrition. Plant Physiol 66:97–100. https://doi.org/10.1104/pp.66.1.97
Boutton TW, Harrison AT, Smith BN (1980) Distribution of biomass of species differing in photosynthetic pathway along an altitudinal transect in southeastern Wyoming grassland. Oecologia 45:287–298. https://doi.org/10.1007/BF00540195
Bräutigam A, Gowik U (2016) Photorespiration connects C3 and C4 photosynthesis. J Exp Bot 67:2953–2962. https://doi.org/10.1093/jxb/erw056
Brown RH (1980) Photosynthesis of grass species differing in carbon dioxide fixation pathways: IV. Analysis of reduced oxygen response in Panicum milioides and Panicum schenckii. Plant Physiol 65:346–349. https://doi.org/10.1104/pp.65.2.346
Brown RH, Brown WV (1975) Photosynthetic characteristics of Panicum milioides, a species with reduced photorespiration. Crop Sci 15:681–685. https://doi.org/10.2135/cropsci1975.0011183X001500050020x
Brown RH, Hattersley PW (1989) Leaf anatomy of C3–C4 species as related to evolution of C4 photosynthesis. Plant Physiol 91:1543–1550. https://doi.org/10.1104/pp.91.4.1543
Brown RH, Morgan JA (1980) Photosynthesis of grass species differing in carbon dioxide fixation pathways: VI. Differential effects of temperature and light intensity on photorespiration in C3, C4, and intermediate species. Plant Physiol 66:541–544. https://doi.org/10.1104/pp.66.4.541
Brown RH, Simmons RE (1979) Photosynthesis of grass species differing in CO2 fixation pathways. I. Water-use efficiency. Crop Sci 19:375–379. https://doi.org/10.2135/cropsci1979.0011183X001900030025x
Brown RH, Bouton JH, Rigsby L, Rigler M (1983) Photosynthesis of grass species differing in carbon dioxide fixation pathways: VIII. Ultrastructural characteristics of Panicum species in the Laxa group. Plant Physiol 71:425–431. https://doi.org/10.1104/pp.71.2.425
Caldwell MM, White RS, Moore RT, Camp LB (1977) Carbon balance, productivity, and water use of cold-winter desert shrub communities dominated by C3 and C4 species. Oecologia 29:275–300. https://doi.org/10.1007/BF00345803
Chastain CJ, Chollet R (1989) Interspecific variation in assimilation of 14CO2 into C4 acids by leaves of C3, C4 and C3–C4 intermediate Flaveria species near the CO2 compensation concentration. Planta 179:81–88. https://doi.org/10.1007/BF00395774
Cheng S-H, Moore BD, Edwards GE, Ku MSB (1988) Photosynthesis in Flaveria brownii, a C4 -like species: leaf anatomy, characteristics of CO2 exchange, compartmentation of photosynthetic enzymes, and metabolism of 14CO2. Plant Physiol 87:867–873. https://doi.org/10.1104/pp.87.4.867
Christin P-A, Freckleton RP, Osborne CP (2010) Can phylogenetics identify C4 origins and reversals? Trends Ecol Evol 25:403–409. https://doi.org/10.1016/j.tree.2010.04.007
Christin P-A, Sage TL, Edwards EJ et al (2011) Complex evolutionary transitions and the significance of C3–C4 intermediate forms of photosynthesis in Molluginaceae. Evolution 65:643–660. https://doi.org/10.1111/j.1558-5646.2010.01168.x
Christin P-A, Wallace MJ, Clayton H et al (2012) Multiple photosynthetic transitions, polyploidy, and lateral gene transfer in the grass subtribe Neurachninae. J Exp Bot 63:6297–6308. https://doi.org/10.1093/jxb/ers282
Christin P-A, Osborne CP, Chatelet DS et al (2013) Anatomical enablers and the evolution of C4 photosynthesis in grasses. Proc Natl Acad Sci USA 110:1381–1386. https://doi.org/10.1073/pnas.1216777110
Christin P-A, Arakaki M, Osborne CP et al (2014) Shared origins of a key enzyme during the evolution of C4 and CAM metabolism. J Exp Bot 65:3609–3621. https://doi.org/10.1093/jxb/eru087
Danila FR, Quick WP, White RG et al (2018) Multiple mechanisms for enhanced plasmodesmata density in disparate subtypes of C4 grasses. J Exp Bot 69:1135–1145. https://doi.org/10.1093/jxb/erx456
Dickinson CE, Dodd JL (1976) Phenological pattern in the shortgrass prairie. Am Midl Nat 96:367. https://doi.org/10.2307/2424076
Downton WJ (1971) Adaptive and evolutionary aspects of C4 photosynthesis. In: Hatch MD, Osmond CB, Slatyer RO (eds) Photosynthesis and photorespiration. Wiley Interscience, New York, pp 3–32
Downton WJS, Tregunna EB (1968) Carbon dioxide compensation—its relation to photosynthetic carboxylation reactions, systematics of the Gramineae, and leaf anatomy. Can J Bot 46:207–215. https://doi.org/10.1139/b68-035
Dunning LT, Moreno-Villena JJ, Lundgren MR et al (2019) Key changes in gene expression identified for different stages of C4 evolution in Alloteropsis semialata. J Exp Bot 70:3255–3268. https://doi.org/10.1093/jxb/erz149
Edwards GE, Ku MS (1987) Biochemistry of C3–C4 intermediates. In: Hatch MD, Boardman NK (eds) The Biochemistry of Plants, vol 10. Academic Press, New York, pp 275–325
Edwards GE, Ku MSB, Hatch MD (1982) Photosynthesis in Panicum milioides, a species with reduced photorespiration. Plant Cell Physiol 23:1185–1195. https://doi.org/10.1093/oxfordjournals.pcp.a076460
Ehleringer J (1978) Implications of quantum yield differences on distributions of C3 and C4 grasses. Oecologia 31:255–267. https://doi.org/10.1007/BF00346246
Ehleringer J, Pearcy R (1983) Variation in quantum yield for CO2 uptake among C3 and C4 plants. Plant Physiol 73:555–559. https://doi.org/10.1104/pp.73.3.555
Ehleringer J, Sage R, Flanagan L, Pearcy R (1991) Climate change and the evolution of C4 photosynthesis. Trends Ecol Evol 6:95–99. https://doi.org/10.1016/0169-5347(91)90183-X
Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 40:503–537. https://doi.org/10.1146/annurev.pp.40.060189.002443
Fisher AE, McDade LA, Kiel CA et al (2015) Evolutionary history of Blepharis (Acanthaceae) and the origin of C4 photosynthesis in section Acanthodium. Int J Plant Sci 176:770–790. https://doi.org/10.1086/683011
Furbank RT (2016) Walking the C4 pathway: past, present, and future. J Exp Bot 67:4057–4066. https://doi.org/10.1093/jxb/erw161
Gowik U, Westhoff P (2011) The path from C3 to C4 photosynthesis. Plant Physiol 155:56–63. https://doi.org/10.1104/pp.110.165308
Griffiths H, Weller G, Toy LFM, Dennis RJ (2013) You’re so vein: bundle sheath physiology, phylogeny and evolution in C3 and C4 plants: origins and function of bundle sheath in C3 plants. Plant Cell Environ 36:249–261. https://doi.org/10.1111/j.1365-3040.2012.02585.x
Harvey P, Pagel MD (1991) The comparative method in evolutionary biology. Oxford University Press, Oxford
Hatch M, Slack C (1966) Photosynthesis by sugar-cane leaves. A new carboxylation reaction and the pathway of sugar formation. Biochem J 101:103–111. https://doi.org/10.1042/bj1010103
Heckmann D, Schulze S, Denton A et al (2013) Predicting C4 photosynthesis evolution: modular, Individually adaptive steps on a Mount Fuji fitness landscape. Cell 153:1579–1588. https://doi.org/10.1016/j.cell.2013.04.058
Henderson S, Caemmerer S, Farquhar G (1992) Short-term measurements of carbon isotope discrimination in several C4 Species. Funct Plant Biol 19:263. https://doi.org/10.1071/PP9920263
Holaday AS, Shieh Y-J, Lee KW, Chollet R (1981) Anatomical, ultrastructural and enzymatic studies of leaves of Moricandia arvensis, a C3–C4 intermediate species. Biochim Biophys Acta Bioenerg 637:334–341. https://doi.org/10.1016/0005-2728(81)90172-9
Holaday AS, Lee KW, Chollet R (1984) C3–C4 intermediate species in the genus Flaveria: leaf anatomy, ultrastructure, and the effect of O2 on the CO2 compensation concentration. Planta 160:25–32. https://doi.org/10.1007/BF00392462
Huxman TE, Monson RK (2003) Stomatal responses of C3, C3–C4 and C4Flaveria species to light and intercellular CO2 concentration: implications for the evolution of stomatal behaviour. Plant Cell Environ 26:313–322. https://doi.org/10.1046/j.1365-3040.2003.00964.x
Hylton CM, Rawsthorne S, Smith AM et al (1988) Glycine decarboxylase is confined to the bundle-sheath cells of leaves of C3–C4 intermediate species. Planta 175:452–459. https://doi.org/10.1007/BF00393064
Kadereit G, Bohley K, Lauterbach M et al (2017) C3–C4 intermediates may be of hybrid origin—a reminder. New Phytol 215:70–76. https://doi.org/10.1111/nph.14567
Kanai R, Kashiwagi M (1975) Panicum milioides, a Gramineae plant having Kranz leaf anatomy without C4-photosynthesis. Plant Cell Physiol. https://doi.org/10.1093/oxfordjournals.pcp.a075187
Kemp PR, Williams GJ (1980) A physiological basis for niche separation between Agropyron smithii (C3) and Bouteloua gracilis (C4). Ecology 61:846–858. https://doi.org/10.2307/1936755
Kennedy RA, Laetsch WM (1974) Plant species intermediate for C3, C4 photosynthesis. Science 184:1087–1089. https://doi.org/10.1126/science.184.4141.1087
Kennedy RA, Eastburn JL, Jensen KG (1980) C3–C4 photosynthesis in the genus Mollugo: structure, physiology and evolution of intermediate characteristics. Am J Bot 67:1207–1217. https://doi.org/10.1002/j.1537-2197.1980.tb07753.x
Khoshravesh R, Stinson CR, Stata M et al (2016) C3–C4 intermediacy in grasses: organelle enrichment and distribution, glycine decarboxylase expression, and the rise of C2 photosynthesis. J Exp Bot 67:3065–3078. https://doi.org/10.1093/jxb/erw150
Khoshravesh R, Stata M, Busch FA et al (2020) The evolutionary origin of C4 photosynthesis in the grass subtribe Neurachninae. Plant Physiol 182:566–583. https://doi.org/10.1104/pp.19.00925
Kocacinar F, Mckown AD, Sage TL, Sage RF (2008) Photosynthetic pathway influences xylem structure and function in Flaveria (Asteraceae). Plant Cell Environ 31:1363–1376. https://doi.org/10.1111/j.1365-3040.2008.01847.x
Kortschak HP, Hartt CE, Burr GO (1965) Carbon dioxide fixation in sugarcane leaves. Plant Physiol 40:209–213. https://doi.org/10.1104/pp.40.2.209
Ku MSB, Edwards GE (1978) Photosynthetic efficiency of Panicum hians and Panicum milioides in relation to C3 and C4 plants. Plant Cell Physiol. https://doi.org/10.1093/oxfordjournals.pcp.a075637
Ku MSB, Monson RK, Littlejohn RO et al (1983) Photosynthetic characteristics of C3–C4 intermediate Flaveria species: I. Leaf anatomy, photosynthetic responses to O2 and CO2, and activities of key enzymes in the C3 and C4 pathways. Plant Physiol 71:944–948. https://doi.org/10.1104/pp.71.4.944
Laetsch WM (1971) Chloroplast structural relationship in leaves of C4 plants. In: Hatch MD, Osmond CB, Slatyer RO (eds) Photosynthesis and photorespiration. Wiley Interscience, New York, pp 323–349
Laetsch WM (1974) The C4 syndrome: a structural analysis. Annu Rev Plant Physiol 25:27–52. https://doi.org/10.1146/annurev.pp.25.060174.000331
Leakey ADB (2009) Rising atmospheric carbon dioxide concentration and the future of C4 crops for food and fuel. Proc R Soc B 276:2333–2343. https://doi.org/10.1098/rspb.2008.1517
Lundgren MR, Christin P-A (2017) Despite phylogenetic effects, C3–C4 lineages bridge the ecological gap to C4 photosynthesis. J Exp Bot 68:241–254. https://doi.org/10.1093/jxb/erw451
Lundgren MR, Besnard G, Ripley BS et al (2015) Photosynthetic innovation broadens the niche within a single species. Ecol Lett 18:1021–1029. https://doi.org/10.1111/ele.12484
Lundgren MR, Christin P-A, Escobar EG et al (2016) Evolutionary implications of C3–C4 intermediates in the grass Alloteropsis semialata. Plant Cell Environ 39:1874–1885. https://doi.org/10.1111/pce.12665
Lundgren MR, Dunning LT, Olofsson JK et al (2019) C 4 anatomy can evolve via a single developmental change. Ecol Lett 22:302–312. https://doi.org/10.1111/ele.13191
Lyu M-JA, Gowik U, Kelly S et al (2015) RNA-Seq based phylogeny recapitulates previous phylogeny of the genus Flaveria (Asteraceae) with some modifications. BMC Evol Biol 15:116. https://doi.org/10.1186/s12862-015-0399-9
Mallmann J, Heckmann D, Bräutigam A et al (2014) The role of photorespiration during the evolution of C4 photosynthesis in the genus Flaveria. eLife 3:e02478. https://doi.org/10.7554/eLife.02478
McKown AD, Moncalvo J-M, Dengler NG (2005) Phylogeny of Flaveria (Asteraceae) and inference of C4 photosynthesis evolution. Am J Bot 92:1911–1928. https://doi.org/10.3732/ajb.92.11.1911
Melillo JM, Richmond TC, Yohe GW (2014) Climate change impacts in the United States: the third national climate assessment. US Global Change Research Program. https://doi.org/10.7930/J0Z31WJ2
Monson RK (1989a) The relative contributions of reduced photorespiration, and improved water-and nitrogen-use efficiencies, to the advantages of C3–C4 intermediate photosynthesis in Flaveria. Oecologia 80:215–221. https://doi.org/10.1007/BF00380154
Monson RK (1989b) On the Evolutionary pathways resulting in C, photosynthesis and crassulacean acid metabolism (CAM). Adv Ecol Res 19:57–110
Monson RK (1996) The use of phylogenetic perspective in comparative plant physiology and development biology. Ann Mo Bot Gard 83:3. https://doi.org/10.2307/2399963
Monson RK (2003) Gene duplication, neofunctionalization, and the evolution of C4 photosynthesis. Int J Plant Sci 164:S43–S54. https://doi.org/10.1086/368400
Monson RK, Jaeger CH (1991) Photosynthetic characteristics of C3–C4 intermediate Flaveria floridana (Asteraceae) in natural habitats: evidence of advantages to C3–C4 photosynthesis at high leaf temperatures. Am J Bot 78:795–800. https://doi.org/10.1002/j.1537-2197.1991.tb14481.x
Monson RK, Moore BD (1989) On the significance of C3–C4 intermediate photosynthesis to the evolution of C4 photosynthesis. Plant Cell Environ 12(7):689–699. https://doi.org/10.1111/j.1365-3040.1989.tb01629.x
Monson RK, Rawsthorne S (2000) Carbon dioxide assimilation in C3–C4 intermediate plants. In: Leegood RC, Sharkey TD, von Caemmerer S (eds) Photosynthesis: physiology and metabolism. Advances in photosynthesis. Kluwer Academic, Dordrecht, pp 533–550
Monson RK, Williams GJ (1982) A correlation between photosynthetic temperature adaptation and seasonal phenology patterns in the shortgrass prairie. Oecologia 54:58–62. https://doi.org/10.1007/BF00541108
Monson RK, Littlejohn RO, Williams GJ (1983) Photosynthetic adaptation to temperature in four species from the Colorado shortgrass steppe: a physiological model for coexistence. Oecologia 58:43–51. https://doi.org/10.1007/BF00384540
Monson RK, Edwards GE, Ku MSB (1984) C3–C4 intermediate photosynthesis in plants. Bioscience 34:563–574. https://doi.org/10.2307/1309599
Monson RK, Moore Bd, Ku MSB, Edwards GE (1986a) Co-function of C3-and C4-photosynthetic pathways in C3, C4 and C3–C4 intermediate Flaveria species. Planta 168:493–502. https://doi.org/10.1007/BF00392268
Monson RK, Sackschewsky MR, Williams GJ (1986b) Field measurements of photosynthesis, water-use efficiency, and growth in Agropyron smithii (C3) and Bouteloua gracilis (C4) in the Colorado shortgrass steppe. Oecologia 68:400–409. https://doi.org/10.1007/BF01036746
Monson RK, Schuster WS, Ku MSB (1987) Photosynthesis in Flaveria brownii A.M. Powell: a C4-like C3–C4 intermediate. Plant Physiol 85:1063–1067. https://doi.org/10.1104/pp.85.4.1063
Monson RK, Teeri JA, Ku MSB et al (1988) Carbon-isotope discrimination by leaves of Flaveria species exhibiting different amounts of C3-and C4-cycle co-function. Planta 174:145–151. https://doi.org/10.1007/BF00394765
Monson, (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, pp 377–410
Moore Bd, Monson RK, Ku MSB, Edwards GE (1988) Activities of principal photosynthetic and photorespiratory enzymes in leaf mesophyll and bundle sheath protoplasts from the C3–C4 intermediate Flaveria-ramosissima. Plant Cell Physiol 29:999–1006
Moore Bd, Ku MSB, Edwards GE (1989) Expression of C4-like photosynthesis in several species of Flaveria. Plant Cell Environ 12:541–549. https://doi.org/10.1111/j.1365-3040.1989.tb02127.x
Morgan JA, Lecain DR, Mosier AR, Milchunas DG (2001) Elevated CO2 enhances water relations and productivity and affects gas exchange in C3 and C4 grasses of the Colorado shortgrass steppe. Glob Change Biol 7:451–466. https://doi.org/10.1046/j.1365-2486.2001.00415.x
Morgan JA, Pataki DE, Körner C et al (2004) Water relations in grassland and desert ecosystems exposed to elevated atmospheric CO2. Oecologia 140:11–25. https://doi.org/10.1007/s00442-004-1550-2
Morgan JA, LeCain DR, Pendall E et al (2011) C4 grasses prosper as carbon dioxide eliminates desiccation in warmed semi-arid grassland. Nature 476:202–205. https://doi.org/10.1038/nature10274
Mueller KE, Blumenthal DM, Pendall E et al (2016) Impacts of warming and elevated CO2 on a semi-arid grassland are non-additive, shift with precipitation, and reverse over time. Ecol Lett 19:956–966. https://doi.org/10.1111/ele.12634
Muhaidat R, Sage TL, Frohlich MW et al (2011) Characterization of C3–C4 intermediate species in the genus Heliotropium L. (Boraginaceae): anatomy, ultrastructure and enzyme activity. Plant Cell Environ 34:1723–1736. https://doi.org/10.1111/j.1365-3040.2011.02367.x
Ode DJ, Tieszen LL, Lerman JC (1980) The seasonal contribution of C3 and C4 plant species to primary production in a mixed prairie. Ecology 61:1304–1311. https://doi.org/10.2307/1939038
Osborne CP, Sack L (2012) Evolution of C4 plants: a new hypothesis for an interaction of CO2 and water relations mediated by plant hydraulics. Philos Trans R Soc B 367:583–600. https://doi.org/10.1098/rstb.2011.0261
Osmond CB, Winter K, Ziegler H (1982) Functional significance of different pathways of CO2 fixation in photosynthesis. In: Lange OL, Nobel PS, Osmond CB, Ziegler H (eds) Physiological plant ecology II. Springer, Berlin, pp 479–547
Powell AM (1978) Systematics of Flaveria (Flaveriinae-Asteraceae). Ann Mo Bot Gard 65:590. https://doi.org/10.2307/2398862
Rathnam CKM, Chollet R (1979) Photosynthetic carbon metabolism in Panicum milioides, a C3–C4 intermediate species: evidence for a limited C4 dicarboxylic acid pathway of photosynthesis. Biochim Biophys Acta Bioenerg 548:500–519. https://doi.org/10.1016/0005-2728(79)90061-6
Rawsthorne S (1992) C3–C4 intermediate photosynthesis: linking physiology to gene expression. Plant J 2:267–274. https://doi.org/10.1111/j.1365-313X.1992.00267.x
Rawsthorne S, Hylton CM (1991) The relationship between the post-illumination CO2 burst and glycine metabolism in leaves of C3 and C3–C4 intermediate species of Moricandia. Planta 186:122–126. https://doi.org/10.1007/BF00201507
Rawsthorne S, Hylton CM, Smith AM, Woolhouse HW (1988a) Photorespiratory metabolism and immunogold localization of photorespiratory enzymes in leaves of C3 and C3–C4 intermediate species of Moricandia. Planta 173:298–308. https://doi.org/10.1007/BF00401016
Rawsthorne S, Hylton CM, Smith AM, Woolhouse HW (1988b) Distribution of photorespiratory enzymes between bundle-sheath and mesophyll cells in leaves of the C3–C4 intermediate species Moricandia arvensis (L.) DC. Planta 176:527–532. https://doi.org/10.1007/BF00397660
Reyes-Fox M, Steltzer H, Trlica MJ et al (2014) Elevated CO2 further lengthens growing season under warming conditions. Nature 510:259–262. https://doi.org/10.1038/nature13207
Reyes-Fox M, Steltzer H, LeCain DR, McMaster GS (2016) Five years of phenology observations from a mixed-grass prairie exposed to warming and elevated CO2. Sci Data 3:160088. https://doi.org/10.1038/sdata.2016.88
Reyna-Llorens I, Burgess SJ, Reeves G et al (2018) Ancient duons may underpin spatial patterning of gene expression in C4 leaves. Proc Natl Acad Sci USA 115:1931–1936. https://doi.org/10.1073/pnas.1720576115
Rumpho ME, Ku MSB, Cheng S-H, Edwards GE (1984) Photosynthetic characteristics of C3–C4 intermediate Flaveria species: III. Reduction of photorespiration by a limited C4 pathway of photosynthesis in Flaveria ramosissima. Plant Physiol 75:993–996. https://doi.org/10.1104/pp.75.4.993
Rundel PW (1980) The ecological distribution of C4 and C3 grasses in the Hawaiian Islands. Oecologia 45:354–359. https://doi.org/10.1007/BF00540205
Sage RF, Monson RK (eds) (1999) C4 plant biology. Academic Press, San Diego
Sage RF (2001) Environmental and evolutionary preconditions for the origin and diversification of the C4 photosynthetic syndrome. Plant Biol 3:202–213. https://doi.org/10.1055/s-2001-15206
Sage RF (2004) The evolution of C4 photosynthesis. New Phytol 161:341–370. https://doi.org/10.1111/j.1469-8137.2004.00974.x
Sage RF (2016) A portrait of the C4 photosynthetic family on the 50th anniversary of its discovery: species number, evolutionary lineages, and Hall of Fame. J Exp Bot 67:4039–4056. https://doi.org/10.1093/jxb/erw156
Sage RF, Kubien DS (2003) Quo vadis C4? An ecophysiological perspective on global change and the future of C4 plants. Photosynth Res 77:209–225. https://doi.org/10.1023/A:1025882003661
Sage RF, Sage TL (2002) Microsite characteristics of Muhlenbergia richardsonis (Trin.) Rydb., an alpine C4 grass from the White Mountains, California. Oecologia 132:501–508. https://doi.org/10.1007/s00442-002-0959-8
Sage RF, Stata M (2021) Terrestrial CO2-concentrating mechanisms in a high CO2 World. In: Way DA, Ward JM, Becklin KM (eds) Photosynthesis, respiration, and climate change. Springer, Berlin (in press)
Sage RF, Sultmanis S (2016) Why are there no C4 forests? J Plant Physiol 203:55–68. https://doi.org/10.1016/j.jplph.2016.06.009
Sage RF, Sage TL, Pearcy RW, Borsch T (2007) The taxonomic distribution of C4 photosynthesis in Amaranthaceae sensu stricto. Amer J Bot 94:1992–2003. https://doi.org/10.3732/ajb.94.12.1992
Sage RF, Christin P-A, Edwards EJ (2011a) The C4 plant lineages of planet Earth. J Exp Bot 62:3155–3169. https://doi.org/10.1093/jxb/err048
Sage RF, Kocacinar F, Kubien DS (2011b) C4 photosynthesis and temperature. In: Raghavendra AS, Sage RF (eds) C4 Photosynthesis and related CO2 concentrating mechanisms. Springer, Dordrecht, pp 161–195
Sage RF, Sage TL, Kocacinar F (2012) Photorespiration and the evolution of C4 photosynthesis. Annu Rev Plant Biol 63:19–47. https://doi.org/10.1146/annurev-arplant-042811-105511
Sage TL, Busch FA, Johnson DC et al (2013) Initial events during the evolution of C4 photosynthesis in C3 species of Flaveria. Plant Physiol 163:1266–1276. https://doi.org/10.1104/pp.113.221119
Sage RF, Khoshravesh R, Sage TL (2014) From proto-Kranz to C4 Kranz: building the bridge to C4 photosynthesis. J Exp Bot 65:3341–3356. https://doi.org/10.1093/jxb/eru180
Sage RF, Monson RK, Ehleringer JR et al (2018) Some like it hot: the physiological ecology of C4 plant evolution. Oecologia 187:941–966. https://doi.org/10.1007/s00442-018-4191-6
Schulze S, Mallmann J, Burscheidt J et al (2013) Evolution of C4 photosynthesis in the genus Flaveria: establishment of a photorespiratory CO2 pump. Plant Cell 25:2522–2535. https://doi.org/10.1105/tpc.113.114520
Schüssler C, Freitag H, Koteyeva N, Schmidt D, Edwards G, Vosnesenskya E, Kadereit G (2017) Molecular phylogeny and forms of photosynthesis in tribe Salsoleae (Chenopodiaceae). J Exp Bot 68:207–223. https://doi.org/10.1093/jxb/erw432
Schuster WS, Monson RK (1990) An examination of the advantages of C3–C4 intermediate photosynthesis in warm environments. Plant Cell Environ 13:903–912. https://doi.org/10.1111/j.1365-3040.1990.tb01980.x
Stata M, Sage TL, Rennie TD et al (2014) Mesophyll cells of C4 plants have fewer chloroplasts than those of closely related C3 plants. Plant Cell Environ 37:2587–2600. https://doi.org/10.1111/pce.12331
Stata M, Sage TL, Hoffmann N et al (2016) Mesophyll chloroplast investment in C3, C4 and C2 species of the genus Flaveria. Plant Cell Physiol 57:904–918. https://doi.org/10.1093/pcp/pcw015
Stata M, Sage TL, Sage RF (2019) Mind the gap: the evolutionary engagement of the C4 metabolic cycle in support of net carbon assimilation. Curr Opin Plant Biol 49:27–34. https://doi.org/10.1016/j.pbi.2019.04.008
Taiz L, Zeiger E, Møller IM, Murphy AS (eds) (2015) Plant physiology and development, 6th edn. Sinauer Associates Inc., Sunderland
Teeri JA, Stowe LG (1976) Climatic patterns and the distribution of C4 grasses in North America. Oecologia 23:1–12. https://doi.org/10.1007/BF00351210
Tieszen LL, Senyimba MM, Imbamba SK, Troughton JH (1979) The distribution of C3 and C4 grasses and carbon isotope discrimination along an altitudinal and moisture gradient in Kenya. Oecologia 37:337–350. https://doi.org/10.1007/BF00347910
Vogan PJ, Sage RF (2011) Water-use efficiency and nitrogen-use efficiency of C3–C4 intermediate species of Flaveria Juss. (Asteraceae): Water- and nitrogen-use in Flaveria. Plant Cell Environ 34:1415–1430. https://doi.org/10.1111/j.1365-3040.2011.02340.x
Vogan PJ, Sage RF (2012) Effects of low atmospheric CO2 and elevated temperature during growth on the gas exchange responses of C3, C3–C4 intermediate, and C4 species from three evolutionary lineages of C4 photosynthesis. Oecologia 169:341–352. https://doi.org/10.1007/s00442-011-2201-z
von Caemmerer S (1989) A model of photosynthetic CO2 assimilation and carbon-isotope discrimination in leaves of certain C3–C4 intermediates. Planta 178:463–474. https://doi.org/10.1007/BF00963816
von Caemmerer S (1992) Carbon isotope discrimination in C3–C4 intermediates. Plant Cell Environ 15:1063–1072
von Caemmerer S, Hubick KT (1989) Short-term carbon-isotope discrimination in C3–C4 intermediate species. Planta 178:475–481. https://doi.org/10.1007/BF00963817
Voznesenskaya EV, Koteyeva NK, Akhani H et al (2013) Structural and physiological analyses in Salsoleae (Chenopodiaceae) indicate multiple transitions among C3, intermediate, and C4 photosynthesis. J Exp Bot 64:3583–3604. https://doi.org/10.1093/jxb/ert191
Williams GJ (1974) Photosynthetic Adaptation to temperature in C3 and C4 grasses: a possible ecological role in the shortgrass prairie. Plant Physiol 54:709–711. https://doi.org/10.1104/pp.54.5.709
Williams GJ, Markley JL (1973) Photosynthetic pathway type of North American shortgrass prairie species and some ecological implications. Photosynthetica 7:262–270
Williams BP, Johnston IG, Covshoff S, Hibberd JM (2013) Phenotypic landscape inference reveals multiple evolutionary paths to C4 photosynthesis. eLife 2:e00961. https://doi.org/10.7554/eLife.00961
Winter K, Usuda H, Tsuzuki M et al (1982) Influence of nitrate and ammonia on photosynthetic characteristics and leaf anatomy of Moricandia arvensis. Plant Physiol 70:616–625. https://doi.org/10.1104/pp.70.2.616
Yorimitsu Y, Kadosono A, Hatakeyama Y et al (2019) Transition from C3 to proto-Kranz to C3–C4 intermediate type in the genus Chenopodium (Chenopodiaceae). J Plant Res 132:839–855. https://doi.org/10.1007/s10265-019-01135-5
Acknowledgements
This manuscript is published as part of a special issue in Oecologia honoring the scientific achievements of Professor Russ Monson. I thank him for sharing stories of his C4 adventures, and for feedback on this manuscript. I also thank Matt Stata for help preparing figures. Preparation of this work was supported by Discovery Grant RGPIN-2017-06476 from the Natural Sciences and Engineering Research Council of Canada.
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RFS designed and wrote the manuscript in its entirety with the exception of Textbox 1 which is a verbatim copy of an e-mail to RFS from Russ Monson on May 22, 2020.
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Sage, R.F. Russ Monson and the evolution of C4 photosynthesis. Oecologia 197, 823–840 (2021). https://doi.org/10.1007/s00442-021-04883-1
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DOI: https://doi.org/10.1007/s00442-021-04883-1