Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Possible involvement of phosphoenolpyruvate carboxylase and NAD-malic enzyme in response to drought stress. A case study: a succulent nature of the C4-NAD-ME type desert plant, Salsola lanata (Chenopodiaceae)

Zhibin Wen A and Mingli Zhang A B C
+ Author Affiliations
- Author Affiliations

A Key Laboratory of Biogeography and Bioresource in Arid Land, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, CN-830011 Urumqi, China.

B Institute of Botany, Chinese Academy of Sciences, CN-100093 Beijing, China.

C Corresponding author. Email: zhangml@ibcas.ac.cn

Functional Plant Biology - https://doi.org/10.1071/FP16430
Submitted: 9 December 2016  Accepted: 12 August 2017   Published online: 2 October 2017

Abstract

The co-ordination between the primary carboxylating enzyme phosphoenolpyruvate carboxylase (PEPC) and the further decarboxylating enzymes is crucial to the efficiency of the CO2-concentrating mechanism in C4 plants, and investigations on more types of C4 plants are needed to fully understand their adaptation mechanisms. In this study we investigated the effect of drought on carboxylating enzyme PEPC, and the further decarboxylating NAD-malic enzyme (NAD-ME) of Salsola lanata Pall. (Chenopodiaceae) – an annual succulent C4-NAD-ME subtype desert plant. We investigated enzyme activity at the transcriptional level with real-time quantitative PCR and at the translational level by immunochemical methods, and compared S. lanata with other forms of studied C4 plants under drought stress. Results showed that only severe stress limited PEPC enzyme activity (at pH 8.0) of S. lanata significantly. Considering that PEPC enzyme activity (at pH 8.0) was not significantly affected by phosphorylation, the decrease of PEPC enzyme activity (at pH 8.0) of S. lanata under severe stress may be related with decreased PEPC mRNA. The suggestion of increased phosphorylation of the PEPC enzyme in plants under moderate stress was supported by the ratio of PEPC enzyme activity at pH 7.3/8.0, as PEPC enzyme is inhibited by L-malate and the evidence of the 50% inhibiting concentration of L-malate. NAD-ME activity decreased significantly under moderate and severe stress, and coincided with a change of leaf water content rather than the amount of α-NAD-ME mRNA and protein. Leaf dehydration may cause the decrease of NAD-ME activity under water stress. Compared with other C4 plants, the activities of PEPC and NAD-ME of S. lanata under drought stress showed distinct features.

Additional keywords: C4 photosynthesis, drought stress, phosphoenolpyruvate carboxylase.


References

Alfonso SU, Brüggemann W (2012) Photosynthetic responses of C3 and three C4 species of the genus Panicum (s.l.) with different metabolic subtypes to drought stress. Photosynthesis Research 112, 175–191.
Photosynthetic responses of C3 and three C4 species of the genus Panicum (s.l.) with different metabolic subtypes to drought stress.CrossRef | 1:CAS:528:DC%2BC38Xht1ais77K&md5=df8a0b45fe7308771d9bd1acf37bde89CAS |

Babayev H, Mehvaliyeva U, Aliyeva M, Feyziyev Y, Guliyev N (2014) The study of NAD-malic enzyme in Amaranthus cruentus L. under drought. Plant Physiology and Biochemistry 81, 84–89.
The study of NAD-malic enzyme in Amaranthus cruentus L. under drought.CrossRef | 1:CAS:528:DC%2BC2cXhtF2nu7Y%3D&md5=038bf4e7f36feb8c4636bc38ca96845cCAS |

Bakrim N, Echevarria C, Cretin C, Arrio-Dupont M, Pierre JN, Vidal J, Chollet R, Gadal P (1992) Regulatory phosphorylation of Sorghum leaf phosphoenolpyruvate carboxylase. Identification of the protein-serine kinase and some elements of the signal-transduction cascade. European Journal of Biochemistry 204, 821–830.
Regulatory phosphorylation of Sorghum leaf phosphoenolpyruvate carboxylase. Identification of the protein-serine kinase and some elements of the signal-transduction cascade.CrossRef | 1:CAS:528:DyaK38XhsVKlsr8%3D&md5=98c89803d0a31c03b173a7a5f6839a0cCAS |

Becker TW, Fock HP (1986) Effects of water stress on the gas exchange, the activities of some enzymes of carbon and nitrogen metabolism, and on the pool sizes of some organic acids in maize leaves. Photosynthesis Research 8, 175–181.
Effects of water stress on the gas exchange, the activities of some enzymes of carbon and nitrogen metabolism, and on the pool sizes of some organic acids in maize leaves.CrossRef | 1:CAS:528:DyaL28XktVektrc%3D&md5=b552c39e50eeeab44f3ef753ab2cf330CAS |

Bernardes da Silva A, Arrabaça MC, Marques da Silva J (2001) Effect of rapid dehydration on the activity of PEPC from the C4 grass Paspalum dilatatum. In ‘PS2001 proceedings of the 12th international congress on photosynthesis’. pp. 1–4. (CSIRO Publishing: Melbourne)

Boyer JS (1982) Plant productivity and environment. Science 218, 443–448.
Plant productivity and environment.CrossRef | 1:STN:280:DC%2BC3cvjvVahuw%3D%3D&md5=06f90b757fd0bacf104d39f12b98707eCAS |

Canellas PF, Wedding RT (1984) Kinetic properties of NAD malic enzyme from cauliflower. Archives of Biochemistry and Biophysics 229, 414–425.
Kinetic properties of NAD malic enzyme from cauliflower.CrossRef | 1:CAS:528:DyaL2cXhtFOju7c%3D&md5=2ee03d31a2de1f37aab02d34fb10e074CAS |

Carmo-Silva AE, Soares AS, Marques da Silva J, Bernardes da Silva A, Keys AJ, Arrabaça MC (2007) Photosynthetic responses of three C4 grasses of metabolic subtypes to water deficit. Functional Plant Biology 34, 204–213.
Photosynthetic responses of three C4 grasses of metabolic subtypes to water deficit.CrossRef | 1:CAS:528:DC%2BD2sXjsVCisr0%3D&md5=34b028504b15d134821d87a6ef2d992fCAS |

Carmo-Silva AE, Bernardes da Silva A, Keys AJ, Parry MAJ, Arrabaça MC (2008) The activities of PEPC carboxylase and the C4 acid decarboxylases are little changed by drought stress in three C4 grasses of different subtypes. Photosynthesis Research 97, 223–233.
The activities of PEPC carboxylase and the C4 acid decarboxylases are little changed by drought stress in three C4 grasses of different subtypes.CrossRef | 1:CAS:528:DC%2BD1cXhtFWitLvL&md5=1b2274a83cf663bce07d2e654af3fcb0CAS |

Chen L, Zhong HY, Kuang JF, Li JG, Lu WJ, Chen JY (2011) Validation of reference genes for RT-qPCR studies of gene expression in banana fruit under different experimental conditions. Planta 234, 377–390.
Validation of reference genes for RT-qPCR studies of gene expression in banana fruit under different experimental conditions.CrossRef | 1:CAS:528:DC%2BC3MXptlyjt7k%3D&md5=17bc621d8ca0498ca482e2482ce6487dCAS |

Chollet R, Vidal J, O’Leary MH (1996) Phosphoenolpyruvate carboxylase: a ubiquitous, highly regulated enzyme in plants. Annual Review of Plant Physiology and Plant Molecular Biology 47, 273–298.
Phosphoenolpyruvate carboxylase: a ubiquitous, highly regulated enzyme in plants.CrossRef | 1:CAS:528:DyaK28XjtlWgsbc%3D&md5=3cb7251181353b9bd2db79265ca6dbffCAS |

Cornic G, Fresneau C (2002) Photosynthetic carbon reduction and oxidation cycles are the main electron sinks for photosystem II activity during a mild drought. Annals of Botany 89, 887–894.
Photosynthetic carbon reduction and oxidation cycles are the main electron sinks for photosystem II activity during a mild drought.CrossRef | 1:CAS:528:DC%2BD38XlsVeitLY%3D&md5=9de40c100d348f0524c37123315512c4CAS |

Doubnerová V, Ryšlavá H (2011) What can enzymes of C4 photosynthesis do for C3 plants under stress? Plant Science 180, 575–583.
What can enzymes of C4 photosynthesis do for C3 plants under stress?CrossRef |

Doubnerová Hýsková V, Miedzińska L, Dobrá J, Vankova R, Ryšlavá H (2014) Phosphoenolpyruvate carboxylase, NADP-malic enzyme, and pyruvate, phosphate dikinase are involved in the acclimation of Nicotiana tabacum L. to drought stress. Journal of Plant Physiology 171, 19–25.
Phosphoenolpyruvate carboxylase, NADP-malic enzyme, and pyruvate, phosphate dikinase are involved in the acclimation of Nicotiana tabacum L. to drought stress.CrossRef |

Du YC, Kawamitsu Y, Nosa A, Hiyane S, Murayama S, Murayama S, Muraya S, Wasano K, Uchida Y (1996) Effects of water stress on carbon exchange rate and activities of photosynthetic enzyme in leaves of sugarcane (Saccharum sp.). Functional Plant Biology 23, 719–726.

Edwards GE, Voznesenskaya EV (2011) C4 photosynthesis: kranz forms and single-cell C4 in terrestrial plants. In ‘C4 photosynthesis and related CO2 concentrating mechanisms’. (Eds AS Raghavendra, RF Sage) pp. 29–61. (Springer)

Flexas J, Bota J, Loreto F, Cornic G, Sharkey TD (2004) Diffusive and metabolic limitations to photosynthesis under drought and salinity in C3 plants. Plant Biology 5, 1–11.

Fontaine V, Cabané M, Dizengremel P (2003) Regulation of phosphoenolpyruvate carboxylase in Pinus halepensis needles submitted to ozone and water stress. Physiologia Plantarum 117, 445–452.
Regulation of phosphoenolpyruvate carboxylase in Pinus halepensis needles submitted to ozone and water stress.CrossRef | 1:CAS:528:DC%2BD3sXjtlOltLs%3D&md5=5279e21d9e2e43d6e130eff06267d472CAS |

Ghannoum O (2009) C4 photosynthesis and water stress. Annals of Botany 103, 635–644.
C4 photosynthesis and water stress.CrossRef | 1:CAS:528:DC%2BD1MXktVGmsr8%3D&md5=ca51ca0da5f76501e076338a3291b756CAS |

González M, Sánchez R, Cejudo FJ (2003) Abiotic stresses affecting water balance induce phosphoenolpyruvate carboxylase expression in roots of wheat seedlings. Planta 216, 985–992.

Gowik U, Westhoff P (2011) C4-Phosphoenolpyruvate carboxylase. In ‘C4 photosynthesis and related CO2 concentrating mechanisms’. (Eds AS Raghavendra, RF Sage) pp. 257–275. (Springer)

Grover SD, Wedding RT (1982) Kinetic ramifications of the association-dissociation behavior of NAD malic enzyme: a possible regulatory mechanism. Plant Physiology 70, 1169–1172.
Kinetic ramifications of the association-dissociation behavior of NAD malic enzyme: a possible regulatory mechanism.CrossRef | 1:CAS:528:DyaL38XmtFWmsrY%3D&md5=6314f8bfb914888ae9d6dff6dfc3e72eCAS |

Gutierrez M, Gracen VE, Edwards GE (1974) Biochemical and cytological relationships in C4 plants. Planta 119, 279–300.
Biochemical and cytological relationships in C4 plants.CrossRef | 1:CAS:528:DyaE2MXivVOltg%3D%3D&md5=a5d2e362086b7b0450c323640303debaCAS |

Hamalainen H, Tubman J, Vikman S, Kyrölä T, Ylikoski E, Warrington J, Lahesmaa R (2001) Identification and validation of endogenous reference genes for expression profiling of T helper cell differentiation by quantitative real-time RT-PCR. Analytical Biochemistry 299, 63–70.
Identification and validation of endogenous reference genes for expression profiling of T helper cell differentiation by quantitative real-time RT-PCR.CrossRef | 1:CAS:528:DC%2BD3MXos1ant70%3D&md5=b0baa579372164f327da0730cf954281CAS |

Hatch MD (1987) C4 photosynthesis: a unique blend of modified biochemistry, anatomy and ultrastructure. Biochimica et Biophysica Acta 895, 81–106.
C4 photosynthesis: a unique blend of modified biochemistry, anatomy and ultrastructure.CrossRef | 1:CAS:528:DyaL1MXjs1Oisw%3D%3D&md5=c082d08c9887db68ab4d35c783baae49CAS |

Hatch MD, Kagawa T, Craig S (1975) Subdivision of C4-pathway species based on differing C4 acid decarboxylating systems and ultrastructural features. Australian Journal of Plant Physiology 2, 111–128.
Subdivision of C4-pathway species based on differing C4 acid decarboxylating systems and ultrastructural features.CrossRef | 1:CAS:528:DyaE2MXksVShtLg%3D&md5=5d351cd83861b17576e31228fa2e0a60CAS |

Hatch MD, Tsuzuki M, Edwards GE (1982) Determination of NAD+ malic enzymes in leaves of C4 plants: effects of malate dehydrogenase and other factors. Plant Physiology 69, 483–491.
Determination of NAD+ malic enzymes in leaves of C4 plants: effects of malate dehydrogenase and other factors.CrossRef | 1:CAS:528:DyaL38XhsFOru7w%3D&md5=4b0b7df2f7a0c8df889e93f88669b86dCAS |

IPCC (2007) Technical summary. In ‘Climate change 2007: the physical science basis. Contribution of Working Group I to the fourth assessment report of the intergovernmental panel on climate change’. (Eds S Solomon, D Qin, M Manning, Z Chen, M Marquis, KB Averyt, M Tignor, HL Miller) pp. 1–70. (Cambridge University Press: Cambridge, UK)

Jian B, Liu B, Bi Y, Hou W, Wu C, Han T (2008) Validation of internal control for gene expression study in soybean by quantitative real-time PCR. BMC Molecular Biology 9, 59
Validation of internal control for gene expression study in soybean by quantitative real-time PCR.CrossRef |

Kadereit G, Borsch T, Weising K, Freitag H (2003) Phylogeny of Amaranthaceae and Chenopodiaceae and the evolution of C4 photosynthesis. International Journal of Plant Sciences 164, 959–986.
Phylogeny of Amaranthaceae and Chenopodiaceae and the evolution of C4 photosynthesis.CrossRef | 1:CAS:528:DC%2BD2cXhs1SgtLw%3D&md5=e1af28f5c3f2f445cbf85d739e1a3009CAS |

Koteyeva NK, Voznesenskaya EV, Berry JO, Chuong SDX, Franceschi VR, Edwards GE (2011) Development of structural and biochemical characteristics of C4 photosynthesis in two types of Kranz anatomy in genus Suaeda (family Chenopodiaceae). Journal of Experimental Botany 62, 3197–3212.
Development of structural and biochemical characteristics of C4 photosynthesis in two types of Kranz anatomy in genus Suaeda (family Chenopodiaceae).CrossRef | 1:CAS:528:DC%2BC3MXnsFWjtLc%3D&md5=3a1908705f0aba9cb3d6f9f04f70abbbCAS |

Koteyeva NK, Voznesenskaya EV, Edwards GE (2015) An assessment of the capacity for phosphoenolpyruvate carboxykinase to contribute to C4 photosynthesis. Plant Science 235, 70–80.
An assessment of the capacity for phosphoenolpyruvate carboxykinase to contribute to C4 photosynthesis.CrossRef | 1:CAS:528:DC%2BC2MXksFWmsrk%3D&md5=ec5c1d8b4445584d15f8c4019e01d260CAS |

Lee SC, Luan S (2012) ABA signal transduction at the crossroad of biotic and abiotic stress responses. Plant, Cell & Environment 35, 53–60.
ABA signal transduction at the crossroad of biotic and abiotic stress responses.CrossRef | 1:CAS:528:DC%2BC38XjvVWht7w%3D&md5=7ac84bbb57c0360db04f49e9935d209eCAS |

Leegood R, Walker BP (1999) Regulation of the C4 pathway. In ‘C4 plant biology’. (Eds RF Sage, RK Monson) pp. 89–131. (Springer)

Li RM, Xie W, Wang SL, Wu QJ, Yang NN, Yang X, Pan H, Zhou X, Bai L, Xu B, Zhou X, Zhang Y (2013) Reference gene selection for qRT-PCR analysis in the sweet potato whitefly, Bemisia tabaci (Hemiptera: Aleyrodidae). PLoS One 8, e53006
Reference gene selection for qRT-PCR analysis in the sweet potato whitefly, Bemisia tabaci (Hemiptera: Aleyrodidae).CrossRef | 1:CAS:528:DC%2BC3sXhtFakt7c%3D&md5=d4961ab1212ac0f5d43cd2e5ad15ffabCAS |

Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method. Methods 25, 402–408.
Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method.CrossRef | 1:CAS:528:DC%2BD38XhtFelt7s%3D&md5=c6e730b8bcaab07d1e52bd2affd3622dCAS |

Long JJ, Wang JL, Berry JO (1994) Cloning and analysis of the C4 photosynthetic NAD-dependent malic enzyme of amaranth mitochondria. Journal of Biological Chemistry 269, 2827–2833.

Marques da Silva J, Arrabaça MC (2004) Photosynthetic enzymes of the C4 grass Setaria sphacelata under water stress: a comparison between rapidly and slowly imposed water deficit. Photosynthetica 42, 43–47.
Photosynthetic enzymes of the C4 grass Setaria sphacelata under water stress: a comparison between rapidly and slowly imposed water deficit.CrossRef |

O’Leary B, Park J, Plaxton WC (2011) The remarkable diversity of plant PEPC (phosphoenolpyruvate carboxylase): recent insights into the physiological functions and post-translational controls of non-photosynthetic PEPCs. The Biochemical Journal 436, 15–34.
The remarkable diversity of plant PEPC (phosphoenolpyruvate carboxylase): recent insights into the physiological functions and post-translational controls of non-photosynthetic PEPCs.CrossRef | 1:CAS:528:DC%2BC3MXlsFGntb8%3D&md5=415bdb5317055fe90df63ee3c7b42772CAS |

Saccardy K, Cornic G, Brulfert J, Reyss A (1996) Effect of drought stress on net CO2 uptake in Zea leaves. Planta 199, 589–595.
Effect of drought stress on net CO2 uptake in Zea leaves.CrossRef | 1:CAS:528:DyaK28XltlWiuro%3D&md5=eeee3f3dda905f97e311d736740a6259CAS |

Sage RF (2001) Environmental and evolutionary preconditions for the origin and diversification of the C4 photosynthetic syndrome. Plant Biology 3, 202–213.
Environmental and evolutionary preconditions for the origin and diversification of the C4 photosynthetic syndrome.CrossRef | 1:CAS:528:DC%2BD3MXlvFGhsLk%3D&md5=391f9dda327f395b70f5d81c3efba357CAS |

Sage RF (2004) The evolution of C4 photosynthesis. New Phytologist 161, 341–370.
The evolution of C4 photosynthesis.CrossRef | 1:CAS:528:DC%2BD2cXhsVymuro%3D&md5=0d5ada2a9d14a18621e05b00f9a32f23CAS |

Sánchez R, Flores A, Cejudo FJ (2006) Arabidopsis phosphoenolpyruvate carboxylase genes encode immunologically unrelated polypeptides and are differentially expressed in response to drought and salt stress. Planta 223, 901–909.
Arabidopsis phosphoenolpyruvate carboxylase genes encode immunologically unrelated polypeptides and are differentially expressed in response to drought and salt stress.CrossRef |

Schulze ED, Ellis R, Schluze W, Trimborn P (1996) Diversity, metabolic types and δ13C carbon isotope ratios in the grass flora of Namibia in relation to growth form, precipitation and habitat conditions. Oecologia 106, 352–369.
Diversity, metabolic types and δ13C carbon isotope ratios in the grass flora of Namibia in relation to growth form, precipitation and habitat conditions.CrossRef |

Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. Journal of Experimental Botany 58, 221–227.
Gene networks involved in drought stress response and tolerance.CrossRef | 1:CAS:528:DC%2BD2sXhtlOlt7w%3D&md5=4871cf223ac27609f0e96e5da0913e7bCAS |

Soares-Cordeiro AS, Carmo-Silva AE, Bernardes da Silva A, Marques da Silva J, Keys AJ, Arrabaça MC (2009) Effects of rapidly imposed water deficit on photosynthetic parameters of three C4 grasses. Photosynthetica 47, 304–308.
Effects of rapidly imposed water deficit on photosynthetic parameters of three C4 grasses.CrossRef | 1:CAS:528:DC%2BD1MXpvFymt7o%3D&md5=1f04365d9cf0abc0dc68cb3db9197bb5CAS |

Su XJ, Fan BG, Yuan LC, Cui XN, Lu SF (2013) Selection and validation of reference genes for quantitative RT-PCR analysis of gene expression in Populus trichocarpa. Chinese Bulletin of Botany 48, 507–518.

Sun ML, Wang YS, Yang DQ, Wei CL, Gao LP, Xia T, Shan Y, Luo Y (2010) Reference genes for real-time fluorescence quantitative PCR in Camellia sinensis. Chinese Bulletin of Botany 45, 579–587.

Tezara W, Mitchell VJ, Driscoll SD, Lawlor DW (1999) Water stress inhibits plant photosynthesis by decreasing coupling factor and ATP. Nature 401, 914–917.
Water stress inhibits plant photosynthesis by decreasing coupling factor and ATP.CrossRef | 1:CAS:528:DyaK1MXntFyltbo%3D&md5=b31d0a0a08c83b146e47603eb008fb97CAS |

Toderich K, Black CC, Juylova E, Kozan O, Mukimov T, Matsuo N (2007) C3/C4 plants in the vegetation of Central Asia, geographical distribution and environmental adaptation in relation to climate. In ‘Climate change and terrestrial carbon sequestration in Central Asia’. (Eds R Lal, M Suleimenov, BA Stewart) pp. 33–66. (Taylor and Francis Group: London)

Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology 3, research0034.1
Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes.CrossRef |

Vidal J, Chollet R (1997) Regulatory phosphorylation of C4 PEP carboxylase. Trends in Plant Science 2, 230–237.
Regulatory phosphorylation of C4 PEP carboxylase.CrossRef |

Voznesenskaya EV, Artyusheva EG, Franceschi VR, Pyankov VI, Kiirats O, Ku MSB, Edwards GE (2001) Salsola arbusculiformis, a C3–C4 intermediate in Salsoleae (Chenopodiaceae). Annals of Botany 88, 337–348.
Salsola arbusculiformis, a C3–C4 intermediate in Salsoleae (Chenopodiaceae).CrossRef |

Willeford KO, Wedding RT (1987) Evidence for a multiple subunit composition of plant NAD malic enzyme. Journal of Biological Chemistry 262, 8423–8429.

Willeford KO, Wedding RT (1992) Oligomerization and regulation of higher plant phosphoenolpyruvate carboxylase. Plant Physiology 99, 755–758.
Oligomerization and regulation of higher plant phosphoenolpyruvate carboxylase.CrossRef | 1:CAS:528:DyaK38Xls1Kntrc%3D&md5=215c70089bc808a1addd53a9640e10a4CAS |

Xiao XL, Ma JB, Wang JR, Wu XM, Li PB, Yao YA (2015) Validation of suitable reference genes for gene expression analysis in the halophyte Salicornia europaea by real-time quantitative PCR. Frontiers in Plant Science 5, 788
Validation of suitable reference genes for gene expression analysis in the halophyte Salicornia europaea by real-time quantitative PCR.CrossRef |

Xu M, Zhang B, Su XH, Zhang SG, Huang MR (2011) Reference gene selection for quantitative real-time polymerase chain reaction in Populus. Analytical Biochemistry 408, 337–339.
Reference gene selection for quantitative real-time polymerase chain reaction in Populus.CrossRef | 1:CAS:528:DC%2BC3cXhsVagsLnP&md5=ba74c1baabc16f8325fbf148cad39e0bCAS |

Zhou ZJ, Su PX, Xie TT, Zhang HN, Li SJ (2014) The physiological and biochemical characteristics and environmental adaptability of Reaumuria soongorica in different habitats. Journal of Desert Research 34, 1007–1014.

Zhu GL, Mosyakin SL, Clemants SE (2003). Fam. Chenopodiaceae. In ‘Flora of China. Vol. 5’. (Eds ZY Wu, PH Raven) pp. 351–414. (Science Press: St Louis, MO, USA)



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