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Salsola laricifolia, another C3–C4 intermediate species in tribe Salsoleae s.l. (Chenopodiaceae)

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Abstract

This study identifies Salsola laricifolia as a C3–C4 intermediate in tribe Salsoleae s.l., Chenopodiaceae, and compares S. laricifolia with the previously described C3–C4 intermediates in Salsoleae. Photosynthetic pathway characteristics were studied in four species of this tribe including S. laricifolia, C3 Sympegma regelii, C3–C4 S. arbusculiformis, and C4 S. arbuscula, using the approaches of leaf anatomy and ultrastructure, activities of ribulose 1-5-bisphosphate carboxylase/oxygenase (Rubisco) and PEP carboxylase (PEPC), CO2 compensation point, and immunolocalization of Rubisco, PEPC, and the P-subunit of glycine decarboxylase (GDC). Salsola laricifolia has intermediate features, with near continuous and distinctive Kranz-like cells (KLCs) compared with the C3-Sympegmoid anatomical type and the C3–C4 intermediate S. arbusculiformis, a relatively low CO2 compensation point (30.4 μmol mol−1) and mesophyll (M)-to KLC tissue ratio, mitochondria in KLCs primarily occurring along the centripetal wall, and specific localization of P-protein GDC in the KLCs. The C3-type isotope value (−22.4 ‰), the absence of the clear labeling for PEPC in M cells, and the low activity of the PEPC enzyme (61.5 μmol mg−1 chlorophyll−1 h−1) support the identification of S. laricifolia as a type I C3–C4 intermediate. Although these C3–C4 intermediate species have different structural features, one with discontinuous KL cells and the other with continuous, they have similar characteristics in physiology and biochemistry.

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Abbreviations

Rubisco:

Ribulose 1-5-bisphosphate carboxylase/oxygenase

PEPC:

Phosphoenolpyruvate carboxylase

GDC:

Glycine decarboxylase

KLC:

Kranz-like cell

M:

Mesophyll

BS:

Bundle sheath

KC:

Kranz cell

Г :

CO2 compensation point

A max :

The maximum rate of photosynthesis

δ 13C:

Carbon isotope value

References

  • Akhani H, Edwards G, Roalson EH (2007) Diversification of the old world Salsoleae s.l. (Chenopodiaceae): molecular phylogenetic analysis of nuclear and chloroplast data sets and a revised classification. Int J Plant Sci 168:931–956. doi:10.1086/518263

    Article  CAS  Google Scholar 

  • Bauwe H (2011) Photorespiration: the bridge to C4 photosynthesis. In: Raghavendra AS, Sage RF (eds) C4 photosynthesis and related CO2 concentrating mechanisms. Springer, Heidelberg, pp 81–108. doi:10.1007/978-90-481-9407-0_6

  • Bender MM, Rouhani I, Vines HM, Black CC Jr (1973) 13C/12C ratio changes in Crassulacean acid metabolism plants. Plant Physiol 52:427–430. doi:10.1104/pp.52.5.427

  • Botschantzev VP (1976) Conspectus specierum sectionis Coccosalsola Fenzl generis Salsola L. Nov Sist Vyssh Rast 13:74–102

  • Brown RH, Bouton JH, Rigsby L, Rigler M (1983a) 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. doi:10.1104/pp.71.2.425

  • Brown RH, Hattersley PW (1989) Leaf anatomy of C3–C4 species as related to evolution of C4 photosynthesis. Plant Physiol 91:1543–1550. doi:10.1104/pp.91.4.1543

  • Brown RH, Rigsby LL, Akin DE (1983b) Enclosure of mitochondria by chloroplasts. Plant Physiol 71:437–439. doi:10.1104/pp.71.2.437

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Carolin RC, Jacobs SWL, Vesk M (1975) Leaf structure in Chenopodiaceae. Bot Jahrb Syst 95:226–255

    Google Scholar 

  • Delgado OR, Gallo AG, De La Torre WW (2006) Nueva aportación al conocimiento de las comunidades rupícolas de la isla de Tenerife (islas Canarias): Soncho congesti-Aeonietum holochrysi ass. nova. Vieraea 34:7–16

  • Douce R, Bourguignon J, Neuburger M, Rebeille F (2001) The glycine decarboxylase system: a fascinating complex. Trends Plant Sci 6:167–176. doi:10.1016/S1360-1385(01)01892-1

    Article  CAS  PubMed  Google Scholar 

  • Edwards GE, Ku MSB (1987) Biochemistry of C3–C4 intermediates. In: Hatch MD, Boardman NK (eds) The biochemistry of plants, vol 10., photosynthesisAcademic Press Inc, New York, pp 275–325

    Google Scholar 

  • Edwards GE, Voznesenskaya EV (2011) C4 photosynthesis: Kranz forms and single-cell C4 in terrestrial plants. In: Raghavendra AS, Sage RF (eds) C4 photosynthesis and related CO2 concentrating mechanisms. Springer, Dordrecht, pp 29–61. doi:10.1007/978-90-481-9407-0_4

  • Freitag H, Kadereit G (2014) C3 and C4 leaf anatomy types in Camphorosmeae (Camphorosmoideae, Chenopodiaceae). Plant Syst Evol 300:665–687. doi:10.1007/s00606-013-0912-9

    Article  Google Scholar 

  • Freitag H, Rilke S (1997) Salsola L. (Chenopodiaceae). In: Rechinger KH (ed) Flora Iranica, vol 172. Graz, Akademische Druck und Verlagsanstalt, pp 154–255

    Google Scholar 

  • Gamaley YV (1985) The variations of the Kranz anatomy in Gobi and Karakum desert plants. Bot Zhurn 70:1302–1314

    Google Scholar 

  • Grubov VI (1999) Chenopodiaceae. In: Vassilczenko IT, Grubov VI, Linczevsky IA, Lipshitz SY (eds) Plants of Central Asia, vol 2., Science Publishers IncEnfield, New Hampshire, pp 87–133

    Google Scholar 

  • Iljin MM (1936) Chenopodiaceae. In: Shishkin BK (ed) Flora SSSR, vol 6. Izdatel’stvo Akademii Nauk SSSR, Leningrad, pp 2–354

    Google Scholar 

  • Jacobs SWL (2001) Review of leaf anatomy and ultrastructure in the Chenopodiaceae (Caryophyllales). J Torrey Bot Soc 128:236–253

    Article  Google Scholar 

  • Kadereit G, Ackerly D, Pirie MD (2012) A broader model for C4 photosynthesis evolution in plants inferred from the goosefoot family (Chenopodiaceae s.s.). Proc R Soc B 279:3304–3311. doi:10.1098/rspb.2012.0440

    Article  PubMed Central  PubMed  Google Scholar 

  • Kadereit G, Borsch T, Weising K, Freitag H (2003) Phylogeny of Amaranthaceae and Chenopodiaceae and the evolution of C4 photosynthesis. Int J Plant Sci 164:959–986. doi:10.1086/378649

    Article  CAS  Google Scholar 

  • Kadereit G, Freitag H (2011) Molecular phylogeny of Camphorosmeae (Camphorosmoideae, Chenopodiaceae): implications for biogeography, evolution of C4 photosynthesis and taxonomy. Taxon 60:51–78

    Google Scholar 

  • Kadereit G, Gotzek D, Jacobs S, Freitag H (2005) Origin and age of Australian Chenopodiaceae. Org Divers Evol 5:59–80. doi:10.1016/j.ode.2004.07.002

    Article  Google Scholar 

  • McKown AD, Dengler NG (2007) Key innovations in the evolution of Kranz anatomy and C4 vein pattern in Flaveria (Asteraceae). Am J Bot 94:382–399. doi:10.3732/ajb.94.3.382

    Article  PubMed  Google Scholar 

  • 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 Inc, San Diego, pp 377–410

    Chapter  Google Scholar 

  • 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. Kluwer, Dordrecht, pp 533–550

  • Morgan CL, Turner SR, Rawsthorne S (1993) Coordination of the cell-specific distribution of the four subunits of glycine decarboxylase and of serine hydroxymethyltransferase in leaves of C3–C4 intermediate species from different genera. Planta 190:468–473. doi:10.1007/BF00224785

    Article  CAS  Google Scholar 

  • Muhaidat R, Sage TL, Frohlich MW, Dengler NG, Sage RF (2011) Characterization of C3–C4 intermediate species in the genus Heliotropium L. (Boraginaceae): anatomy, ultrastructure and enzyme activity. Plant Cell Environ 34:1723–1736. doi:10.1111/j.1365-3040.2011.02367.x

    Article  CAS  PubMed  Google Scholar 

  • Pyankov VI, Artyusheva EG, Edwards GE, Black CC Jr, Soltis PS (2001a) Phylogenetic analysis of tribe Salsoleae (Chenopodiaceae) based on ribosomal ITS sequences: implications for the evolution of photosynthesis types. Am J Bot 88:1189–1198

    Article  CAS  PubMed  Google Scholar 

  • Pyankov VI, Ziegler H, Kuz’min A, Edwards GE (2001b) Origin and evolution of C4 photosynthesis in the tribe Salsoleae (Chenopodiaceae) based on anatomical and biochemical types in leaves and cotyledons. Plant Syst Evol 230:43–74

    Article  CAS  Google Scholar 

  • Rawsthorne S (1992) C3–C4 intermediate photosynthesis: linking physiology to gene expression. Plant J 2:267–274. doi:10.1111/j.1365-313X.1992.00267.x

    Article  CAS  Google Scholar 

  • Rawsthorne S, Bauwe H (1998) C3–C4 intermediate photosynthesis. In: Raghavendra AS (ed) photosynthesis. A comprehensive treatise. Cambridge University Press, Cambridge, pp 150–162

    Google Scholar 

  • Rawsthorne S, Hylton CM, Smith AM, Woolhouse HW (1988) Photorespiratory metabolism and immunogold localization of photorespiratory enzymes in leaves of C3 and C3–C4 intermediate species of Moricandia. Planta 173:298–308. doi:10.1007/BF00401016

  • Sage RF (2001) Environmental and evolutionary preconditions for the origin and diversification of the C4 photosynthetic syndrome. Plant Biol 3:202–213. doi:10.1055/s-2001-15206

    Article  CAS  Google Scholar 

  • Sage RF (2004) The evolution of C4 photosynthesis. New Phytol 161:341–370. doi:10.1111/j.1469-8137.2004.00974.x

    Article  CAS  Google Scholar 

  • Sage RF, Christin PA, Edwards EJ (2011a) The C4 plant lineages of planet earth. J Exp Bot 62:3155–3169. doi:10.1093/jxb/err048

  • Sage RF, Li MR, Monson RK (1999) The taxonomic distribution of C4 photosynthesis. In: Sage RF, Monson RK (eds) C4 plant biology. Academic Press Inc, California, USA, pp 551–584

  • Sage TF, Sage RF, Vogan PJ, Rahman B, Johnson DC, Oakley JC, Heckel MA (2011b) The occurrence of C2 photosynthesis in Euphorbia subgenus Chamaesyce (Euphorbiaceae). J Exp Bot 62:3183–3195. doi:10.1093/jxb/err059

  • Schulze ED, Ellis R, Schulze W, Trimborn P, Ziegler H (1996) Diversity, metabolic type and δ 13C carbon isotope ratios in the grass flora of Namibia in relation to growth form, precipitation and habitat conditions. Oecologia 106:352–369. doi:10.1007/BF00334563

    Article  Google Scholar 

  • Ueno O (1992) Immunogold localization of photosynthetic enzymes in leaves of Aristida latifolia, a unique C4 grass with a double chlorenchymatous bundle sheath. Physiol Plant 85:189–196. doi:10.1111/j.1399-3054.1992.tb04722.x

  • Voznesenskaya EV, Artyusheva EG, Franceschi VR, Pyankov VI, Kiirats O, Ku MSB, Edwards GE (2001) Salsola arbusculiformis, a C3–C4 intermediate in Salsoleae (Chenopodiaceae). Ann Bot 88:337–348. doi:10.1006/anbo.2001.1457

    Article  Google Scholar 

  • Voznesenskaya EV, Gamaley YV (1986) The ultrastructural characteristics of leaf types with Kranz-anatomy. Bot Zhurn 71:1291–1307

    Google Scholar 

  • Voznesenskaya EV, Koteyeva NK, Akhani H, Roalson EH, Edwards GE (2013) Structural and physiological analyses in Salsoleae (Chenopodiaceae) indicate multiple transitions among C3, intermediate, and C4 photosynthesis. J Exp Bot 64:3583–3604. doi:10.1093/jxb/ert191

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wen ZB, Zhang ML (2011) Anatomical types of leaves and assimilating shoots and carbon 13C/12C isotope fractionation in Chinese representatives of Salsoleae s.l. (Chenopodiaceae). Flora 206:720–730. doi:10.1016/j.flora.2010.11.015

    Article  Google Scholar 

  • Wen ZB, Zhang ML, Meng HH (2014) Salsola arbusculiformis and S. laricifolia (Chenopodiaceae) in China. Nord J Bot 32:167–175. doi:10.1111/j.1765-1051.2013.00113.x

    Article  Google Scholar 

  • Wen ZB, Zhang ML, Zhu GL, Sanderson SC (2010) Phylogeny of Salsoleae s.l. (Chenopodiaceae) based on DNA sequence data from ITS, psbB-psbH, and rbcL, with emphasis on taxa of northwestern China. Plant Syst Evol 288:25–42. doi:10.1007/s00606-010-0310-5

  • Zhu GL, Mosyakin SL, Clemants SE (2003) Fam. Chenopodiaceae. In: Wu ZY, Raven PH (eds) Flora of China, vol 5. Science Press, St Louis, pp 351–414

    Google Scholar 

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Acknowledgments

We are grateful to contributions made by Dr. Lin Wu and Dr. Xiaobin Zhou (measurement of CO2 compensation points) from the Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences (CAS) (Urumqi, Xinjiang, China), Prof. Peixi Su (measurement of CO2 compensation points) from the Cold and Arid Regions Environmental and Engineering Research Institute, CAS (Lanzhou, Gansu, China), Jianmin Luo (leaf ultrastructure) from Xinjiang University (Urumqi, Xinjiang, China), Prof. Elena V. Voznesenskaya (important comments) from Laboratory of Anatomy and Morphology, V. L. Komarov Botanical Institute of Russian Academy of Sciences (Saint-Petersburg, Russia), and Dr. Stewart C. Sanderson (English improvement) from the Shrub Sciences Laboratory (USDA, Utah, USA). This research was funded by the National Basic Research Program of China (2009CB825104), CAS West Light Foundation (No. XBBS201209), National Natural Science Foundation of China (31300217) and Xinjiang Institute of Ecology and Geography, CAS.

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Wen, Z., Zhang, M. Salsola laricifolia, another C3–C4 intermediate species in tribe Salsoleae s.l. (Chenopodiaceae). Photosynth Res 123, 33–43 (2015). https://doi.org/10.1007/s11120-014-0037-1

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