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Journal of Arid Land
Journal of Arid Land  2024, Vol. 16 Issue (7): 963-982    DOI: 10.1007/s40333-024-0018-y
Research article     
Plasticity of photorespiratory carbon concentration mechanism in Sedobassia sedoides (Pall.) Freitag & G. Kadereit under elevated CO2 concentration and salinity
Zulfira RAKHMANKULOVA1, Elena SHUYSKAYA1, Maria PROKOFIEVA1, Kristina TODERICH2,*()(), Pavel VORONIN1
1Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, Moscow 127276, Russia
2Graduate School of Bioresources, Mie University, 1577 Kurimamachiya, Tsu 514-8507, Japan
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Abstract  

Rising atmospheric CO2 (carbon dioxide) concentrations and salinization are manifestations of climate change that affect plant growth and productivity. Species with an intermediate C3-C4 type of photosynthesis live in a wide range of precipitation, temperature, and soil quality, but are more often found in warm and dry habitats. One of the intermediate C3-C4 photosynthetic type is C2 photosynthesis with a carbon concentration mechanism (CCM) that reassimilates CO2 released via photorespiration. However, the ecological significance under which C2 photosynthesis has advantages over C3 and C4 plants remains largely unexplored. Salt tolerance and functioning of CCM were studied in plants from two populations (P1 and P2) of Sedobassia sedoides (Pall.) Freitag & G. Kadereit Asch. species with C2 photosynthesis exposed to 4 d and 10 d salinity (200 mM NaCl) at ambient (785.7 mg/m3, aCO2) and elevated (1571.4 mg/m3, eCO2) CO2. On the fourth day of salinity, an increase in Na+ content, activity catalase, and superoxide dismutase was observed in both populations. P2 plants showed an increase in proline content and a decrease in photosynthetic enzyme content: rubisco, phosphoenolpyruvate carboxylase (PEPC), and glycine decarboxylase (GDC), which indicated a weakening of C2 and C4 characteristics under salinity. Treatment under 10 d salinity led to an increased Na+ content and activity of cyclic electron flow around photosystem I (PSI CEF), a decreased content of K+ and GDC in both populations. P1 plants showed greater salt tolerance, which was assessed by the degree of reduction in photosynthetic enzyme content, PSI CEF activity, and changes in relative growth rate (RGR). Differences between populations were evident under the combination of eCO2 and salinity. Under long-term salinity and eCO2, more salt-tolerant P1 plants had a higher dry biomass (DW), which was positively correlated with PSI CEF activity. In less salt-tolerant P2 plants, DW correlated with transpiration and dark respiration. Thus, S. sedoides showed a high degree of photosynthetic plasticity under the influence of salinity and eCO2 through strengthening (P1 plants) and weakening C4 characteristics (P2 plants).

Key words： photosystems I and II      carbon-concentrating mechanism      glycine decarboxylase      rubisco      phosphoenolpyruvate carboxylase (PEPC)      cyclic electron flow      salinity stress      drylands     
Received: 09 February 2024      Published: 31 July 2024
Corresponding Authors: * Kristina TODERICH (E-mail: ktoderich@tottori-u.ac.jp, ktoderich@bio.mie-u.ac.jp; ORCID: 0000-0003-2825-7214)
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Zulfira RAKHMANKULOVA
Elena SHUYSKAYA
Maria PROKOFIEVA
Kristina TODERICH
Pavel VORONIN
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Zulfira RAKHMANKULOVA, Elena SHUYSKAYA, Maria PROKOFIEVA, Kristina TODERICH, Pavel VORONIN. Plasticity of photorespiratory carbon concentration mechanism in Sedobassia sedoides (Pall.) Freitag & G. Kadereit under elevated CO2 concentration and salinity. Journal of Arid Land, 2024, 16(7): 963-982.

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http://jal.xjegi.com/10.1007/s40333-024-0018-y     OR     http://jal.xjegi.com/Y2024/V16/I7/963

Habitat Soil type Salt (%) Humus content (%)
1 Chestnut soil 0.11±0.01 1.91±0.24
2 Chestnut soil 0.13±0.01 1.89±0.21
3** Chestnut solonetzic soil 0.27±0.03 0.80±0.15
4 Chestnut solonetzic soil 0.10±0.01 1.95±0.20
5 Solonetz not washed from salts 0.77±0.09 0.88±0.19
6* Crust solonetz not washed from salts 0.98±0.11 1.89±0.22
Table S1 Soil conditions for Sedobassia sedoides (Pall.) Freitag & G. Kadereit populations in the desert steppes of northwestern Caspian Lowland
Parameter aCO2 eCO2
PC1 PC2 PC1 PC2
DW −0.291 0.008 0.335 −0.154
W 0.268 0.147 −0.293 0.302
Pro −0.084 0.282* 0.040 −0.042
Na+ −0.274 −0.032 0.320 0.206
K+ 0.324* 0.126 −0.343* −0.128
K+/Na+ ratio 0.306* 0.068 −0.346* −0.190
PSI −0.265 0.201 0.126 −0.371*
PSII 0.265 −0.101 −0.283 0.065
A 0.090 −0.671* −0.280 0.330
Rd −0.249 −0.153 −0.008 0.413*
E −0.156 −0.572* 0.064 0.495*
WUE 0.246 −0.085 −0.300 −0.020
Rub 0.298 −0.129 −0.231 0.074
PEPC 0.288 −0.049 −0.138 −0.278
GDC 0.309* 0.009 −0.345* −0.198
Table S2 Factor loading of physiological and biochemical parameters on principal component (PC1 and PC2) analysis of S. sedoides from P1 and P2 populations under 4 and10 d NaCl treatments at ambient CO2 (aCO2) and elevated CO2 (eCO2) concentrations
Fig. 1 Effects of 4 and 10 d NaCl-induced salinity at ambient CO2 (aCO2) and elevated CO2 (eCO2) concentrations on biomass and water content in Sedobassia sedoides (Pall.) Freitag & G. Kadereit plants from P1 and P2 populations. (a), fresh biomass; (b), dry biomass and RGR (relative growth rate); (c), water content. Control, plants growing at aCO2; NaCl, plants growing at aCO2+4 d treated by 200 mM NaCl; eCO2, plants growing at eCO2; eCO2+NaCl, plants growing at eCO2+4 d treated by 200 mM NaCl; 2Control, plants growing at aCO2; 2NaCl, plants growing at aCO2+10 d treated by 200 mM NaCl; 2eCO2, plants growing at eCO2; 2eCO2+NaCl, plants growing at eCO2+10 d treated by 200 mM NaCl. DW, dry weight. Different lowercase letters indicate statistically difference among different treatments at P<0.05 level (Tukey's test). Bars are standard errors (n=7). * indicates significant differences between two salinity treatments. The abbreviations and symbols are the same in the following figures.
Fig. 2 Effects of 4 and 10 d NaCl-induced salinity at ambient (aCO2) and elevated (eCO2) CO2 concentrations on apparent A (photosynthesis; a), E (transpiration; b), Rd (dark respiration; c), and WUE (water use efficiency; d) in S. sedoides plants from P1 and P2 populations
Fig. 3 Effects of 4 and 10 d NaCl-induced salinity at ambient CO2 (aCO2) and elevated CO2 (eCO2) concentrations on immunoblot analysis of enzymes (a), rubisco (b), GDC (glycine decarboxylase; c), and PEPC (phosphoenolpyruvate carboxylase; d) contents in S. sedoides plants from P1 and P2 populations
Fig. 4 Effects of 4 and 10 d NaCl-induced salinity at ambient CO2 (aCO2) and elevated CO2 (eCO2) concentrations on photosynthetic parameters in S. sedoides plants from P1 and P2 populations. (a), time of P700 oxidation (cyclic electron flow around photosystem I); (b), Fv/Fm (photosystem II).
Fig. S1 Effect of 4 and 10 d NaCl-induced salinity at ambient (aCO2) and elevated (eCO2) CO2 concentrations on proline (a), Na+ (b), K+ (c) contents, and K+/Na+ ratio (d) in S. sedoides plants from P1 and P2 populations. Control, plants growing at aCO2; NaCl, plants growing at aCO2+4 d treated by 200 mM NaCl; eCO2, plants growing at eCO2; eCO2+NaCl, plants growing at eCO2+4 d treated by 200 mM NaCl; 2Control, plants growing at aCO2; 2NaCl, plants growing at aCO2+10 d treated by 200 mM NaCl; 2eCO2, plants growing at eCO2; 2eCO2+NaCl, plants growing at eCO2+10 d treated by 200 mM NaCl. DW, dry weight. Bars are standard errors (n=7). Different lowercase letters show statistically difference among different treatments at P<0.05 level (Tukey's test). * indicates significant differences between two salinity treatments. The treatments are the same as in the following figure.
Fig. S2 Effect of 4 and 10 d NaCl-induced salinity at ambient CO2 (aCO2) and elevated CO2 (eCO2) concentrations on antioxidant enzymes activity and lipid peroxidation in S. sedoides plants from P1 and P2 populations. (a), APX (ascorbate peroxidase); (b), CAT (catalase); (c), SOD ( superoxide dismutase); (d), MDA (malondialdehyde). AsA, ascorbate; FW, fresh weight.
Fig. 5 Principle component analysis (PCA) (a and b) and multiple correlation (c-f) of physiological and biochemical parameters under 4 and 10 d of NaCl-induced salinity at ambient CO2 (aCO2) and elevated CO2 (eCO2) concentrations of S. sedoides plants from P1 and P2 populations. (a), aCO2; (b), eCO2; (c), P1-aCO2 ; (d), P2-aCO2; (e), P1-eCO2; (f), P2-eCO2. DW, dry weight; W, water content; Pro, proline; PSI, photosystems I; PSII, photosystems II; A, apparent photosynthesis; Rd, dark respiration; E, transpiration; WUE, water use efficiency; Rub, rubisco; PEPC, phosphoenolpyruvate carboxylase; GDC, glycine decarboxylase; GLDP, glycine decarboxylase P protein. The arrows in Figure 5a and b show a gradual change in adaptation mechanisms under 4 and 10 d salinity treatments.
Fig. 6 Stress-induced photosynthetic plasticity of C3-C4 intermediate S. sedoides plants under eCO2 and NaCl treatments. P1 and P2 are two populations of S. sedoides. Green color shows the type of intermediate С3-С4 photosynthesis.
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