Bienertia sinuspersici is one of four known terrestrial plants that perform C4 photosynthesis within individual chlorenchyma cells termed single cell C4 (SCC4) photosynthesis.
All four species are unlike a typical Kranz-type anatomy C4 species which perform photosynthesis with dimorphic chloroplasts in a dual cell scheme in where mesophyll and bundle sheath cells form a wreath-like arrangement around the vascular bundles. Rather, Bienertia sinuspersici and its sister species B. cycloptera, and B. kavirense have developed an unusual means of performing C4 through spatial separation of function between dimorphic chloroplasts located between a central and peripheral cytoplasmic compartment in individual cells. The fourth of the described species, Suaeda aralocaspica, performs C4 photosynthesis in a single cell utilizing a polar arrangement of the dimorphic chloroplasts. The unprecedented occurrence of dimorphic chloroplasts in the same cell with one nucleus raises interesting questions about chloroplast development and organellar communications.
To begin to address some of these questions the Edwards and Dhingra Labs at WSU and the Offermann lab at Leibniz Universität, Hannover, Germany, are in the process of constructing the genome of Bienertia sinuspersici. To take advantage of the different strengths of next-generation sequencing approaches, we are currently working with the Pacific Bioscience RS, Roche 454 GS FLX and Illumina HiSeq 2000 platforms to generate and construct the genome. Bioinformatic pipeline workflows, optimized in the Dhingra lab, are being used to integrate the different sequence outputs from these three platforms into a comprehensive picture of the B. sinuspersici genome.
Offermann S, Friso G, Doroshenk KA, Sun Q, Sharpe RM, Okita TW, Wimmer D, Edwards GE, van Wijk KJ (2015) Developmental and Subcellular Organization of Single-Cell C4 Photosynthesis in Bienertia sinuspersici Determined by Large-Scale Proteomics and cDNA Assembly from 454 DNA Sequencing. Journal of Proteome Research 14: 2090–2108. doi: 10.1021/pr5011907
Lung S-C, Smith MD, Weston JK, Gwynne W, Secord N, Chuong SDX (2014) The C-terminus of Bienertia sinuspersici Toc159 contains essential elements for its targeting and anchorage to the chloroplast outer membrane. Frontiers in Plant Science. doi: 10.3389/fpls.2014.00722
Stutz, S.S., Edwards, G.E. and Cousins, A.B. (2014) Single-cell C4 photosynthesis: efficiency and acclimation of Bienertia sinuspersici to growth under low light. New Phytologist, 202, 220–232.
Rosnow, J.J., Edwards, G.E. and Roalson, E.H. (2014) Positive selection of Kranz and non-Kranz C4 phosphoenolpyruvate carboxylase amino acids in Suaedoideae (Chenopodiaceae). Journal of Experimental Botany, 10.1093/jxb/eru053.
Sharpe, R.M. and Offermann, S. (2014) One decade after the discovery of single-cell C4 species in terrestrial plants: what did we learn about the minimal requirements of C4 photosynthesis? Photosynthesis Research, 119, 169–180.
Rosnow, J., Yerramsetty, P., Berry, J.O., Okita, T.W. and Edwards, G.E. (2014) Exploring mechanisms linked to differentiation and function of dimorphic chloroplasts in the single cell C4 species Bienertia sinuspersici. BMC Plant Biology, 14, 34.
Lung, S.-C. and Chuong, S.D.X. (2012) A Transit Peptide-Like Sorting Signal at the C Terminus Directs the Bienertia sinuspersici Preprotein Receptor Toc159 to the Chloroplast Outer Membrane. THE PLANT CELL ONLINE, 10.1105/tpc.112.096248.
King J, Edwards GE, Cousins AB (2012) The efficiency of the CO2 concentrating mechanism during single-cell C4 photosynthesis. Plant Cell Environment 35: 513-523
Akhani, H., Chatrenoor, T., Dehghani, M., Khoshravesh, R., Mahdavi, P. and Matinzadeh, Z. (2012) A new species of Bienertia (Chenopodiaceae) from Iranian salt deserts: A third species of the genus and discovery of a fourth terrestrial C4 plant without Kranz anatomy. Plant Biosys – Intl J Deal Aspect Plant Biol, 10.1080/11263504.2012.662921.
Lung, S.-C., Yanagisawa, M. and Chuong, S.D. (2012) Isolation of dimorphic chloroplasts from the single-cell C4 species Bienertia sinuspersici. Plant Methods, 8, 8.
Northmore JA, Zhou V, Chuong SDX (2012) Multiple shoot induction and plant regeneration of the single-cell C4 species Bienertia sinuspersici. Plant Cell Tiss Organ Cult 108: 101-109
Offermann S, Okita T, Edwards GE (2011) Resolving the compartmentation and function of C4 photosynthesis in the single-cell C4 species Bienertia sinuspersici. Plant Physiology 155: 1612-1628
Offermann S, Okita TW, Edwards GE (2011) How do single cell C4 species form dimorphic chloroplasts? Plant Signaling & Behavior 6: 762-765
Rosnow J, Offermann S, Park J-H, Okita T, Tarlyn N, Dhingra A, Edwards GE (2011) In vitro cultures and regeneration of Bienertia sinuspersici (Chenopodiaceae) under increasing concentrations of sodium chloride and carbon dioxide. Plant Cell Reports 30: 1541-1553
Akhani H, Chatrenoor T, Dehghani M, Khoshravesh R, Matinzadeh Z (2011) A new species of Bienertia (Chenopodiaceae) from Iranian salt deserts: a third species of the genus and discovery of a fourth terrestrial C4 plant without Kranz anatomy Plant Biosystems in press
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. Advances in Photosynthesis and Respiration, Vol 32 Springer, Dordrecht, The Netherlands, pp 29-61
Leisner CP, Cousins AB, Offermann S, Okita TW, Edwards GE (2010) The effects of salinity on photosynthesis and growth of the single-cell C4 species Bienertia sinuspersici (Chenopodiaceae). Photosynthesis Research 106: 201-214
Park J, Okita TW, Edwards GE (2010) Expression profiling and proteomic analysis of isolated photosynthetic cells of the non-Kranz C4 species Bienertia sinuspersici. Functional plant biology 37: 1-13
Shiu-Cheung L, Yanagisawa M, Chuong SDX (2010 ) Protoplast isolation and transient gene expression in the single-cell C4 species, Bienertia sinuspersici. Plant Cell Reports 30: 473-484
Park J, Okita TW, Edwards GE (2009) Salt tolerant mechanisms in single-cell C4 species Bienertia sinuspersici and Suaeda aralocaspica (Chenopodiaceae). Plant Science 176: 616-626
Park J, Knoblauch M, Okita T, Edwards GE (2009) Structural changes in the vacuole and cytoskeleton are key to development of the two cytoplasmic domains supporting single-cell C4 photosynthesis in Bienertia sinuspersici. Planta 229: 369-382
Akhani H, Lara MV, Ghasemkhani M, Ziegler H, Edwards GE (2009) Does Bienertia cycloptera with the single-cell system of C4 photosynthesis exhibit a seasonal pattern of 13C values in nature similar to co-existing C4 Chenopodiaceae having the dual-cell (Kranz) system? Photosynthesis Research 99: 23-36
Smith ME, Koteyeva NK, Voznesenskaya EV, Okita TW, Edwards GE (2009) Photosynthetic features of non-Kranz type C4 versus Kranz type C4 and C3 species in subfamily Suaedoideae (Chenopodiaceae). Functional Plant Biology 36: 770-782
Lara MV, Offermann S, Smith M, Okita TW, Andreo CS, Edwards GE (2008) Leaf development in the single-cell C4 system in Bienertia sinuspersici: Expression of genes and peptide levels for C4 metabolism in relation to chlorenchyma structure under different light conditions. Plant Physiology 148: 593-610
Boyd CN, Franceschi VR, Chuong SDX, Akhani H, Kiirats O, Smith M, Edwards GE (2007) Flowers of Bienertia cycloptera and Suaeda aralocaspica (Chenopodiaceae) complete the life cycle performing single-cell C4 photosynthesis. Functional plant biology 34: 268-281
Edwards GE, Voznesenskaya EV, Smith M, Koteyeva N, Park Y-I, Park JH, Kiirats O, Okita TW, Chuong SDX (2007) Breaking the Kranz paradigm in terrestrial C4 plants: Does it hold promise for C4 rice? In: Sheehy JE, Mitchell PL, Hardy B (eds) Charting New Pathways to C4 rice International Rice Research Institute, World Scientific, Los Banos, Philippines, pp 249-273
Chuong SDX, Franceschi VR, Edwards GE (2006) The cytoskeleton maintains organelle partitioning required for single-cell C4 photosynthesis in Chenopodiaceae species. The Plant Cell 18: 2207-2223
Kapralov MV, Akhani H, Voznesenskaya E, Edwards G, Franceschi VR, Roalson EH (2006) Phylogenetic relationships in the Salicornioideae /Suaedoideae /Salsoloideae s.l. (Chenopodiaceae) clade and a clarification of the phylogenetic position of Bienertia and Alexandra using multiple DNA sequence datasets. Systematic Botany 31: 571-585.
Kapralov MV, Akhani H, Voznesenskaya EV, Edwards GE, Franceschi V, Roalson EH (2006) Phylogenetic relationships in the Salicornioideae / Suaedoideae / Salsoloideae s.l. (Chenopodiaceae) clade and a clarification of the phylogenetic position of Bienertia and Alexandra using multiple DNA sequence datasets. Systematic Botany 31: 571-585
Lara MV, Chuong SDX, Akhani H, Andreo CS, Edwards GE (2006) Species having C4 single-cell-type photosynthesis in the Chenopodiaceae family evolved a photosynthetic phosphoenolpyruvate carboxylase like that of Kranz-type C4 species. Plant Physiology 142: 673-684
Akhani H, Barroca J, Koteeva N, Voznesenskaya E, Franceschi V, Edwards G, Ghaffari SM, Ziegler H (2005) Bienertia sinuspersici (Chenopodiaceae): a new species from Southwest Asia and discovery of a third terrestrial C4 plant without Kranz anatomy. Systematic Botany 30: 290-301
Voznesenskaya EV, Koteeva NK, Chuong SDX, Akhani H, Edwards GE, Franceschi VR (2005) Differentiation of cellular and biochemical features of the single cell C4 syndrome during leaf development in Bienertia cycloptera (Chenopodiaceae). American Journal of Botany 92: 1784-1795
Voznesenskaya EV, Koteyeva NK, Chuong SDX, Edwards GE, Akhani H, Franceschi VR (2005) Differentiation of cellular and biochemical features of the single cell C4 syndrome during leaf development in Bienertia cycloptera (Chenopodiaceae). American Journal of Botany 92: 1784-1795
Voznesenskaya EV, Franceschi VR, Edwards GE (2004) Light-dependent development of single cell C4 photosynthesis in cotyledons of Borszczowia aralocaspica (Chenopodiaceae) during transformation from a storage to a photosynthetic organ. Annals of Botany 93: 1-11
Edwards GE, Franceschi VR, Voznesenskaya EV (2004) Single cell C4 photosynthesis versus the dual-cell (Kranz) paradigm. Annual Review of Plant Biology 55: 173-196
Akhani H, Ghobadnejhad M, Hashemi SMH (2003) Ecology, biogeography and pollen morphology of Bienertia cycloptera Bunge ex Boiss. (Chenopodiaceae), an enigmatic C4 plant without Kranz anatomy. Plant Biology 5: 167-178