Abstract
Main conclusion
Salt and alkali stress affected the photosynthetic characteristics of Chinese cabbages. A salt-tolerant cultivar maintained its tolerance by ensuring the high ability of photosynthesis. The synthesis of organic acids and carbohydrates in leaves played important roles in improving the photosynthetic capacity of alkali-tolerant plants.
Abstract
Soil salinization has become an increasingly serious ecological problem, which limits the quality and yield of crops. As an important economic vegetable in winter, however, little is known about the response of Chinese cabbage to salt, alkali and salt–alkali stress in photosynthetic characteristics and chloroplast ultrastructure. Thus, two Chinese cabbage cultivars, ‘Qinghua’ (salt-tolerant–alkali-sensitive) and ‘Biyu’ (salt-sensitive–alkali-tolerant) were investigated under stresses to clarify the similarities and differences between salt tolerance and alkali tolerance pathways in Chinese cabbage. We found that the root of Qinghua, the leaf ultrastructure and net photosynthetic rate (Pn), stomatal conductance (Gs), water use efficiency (WUE), maximum photochemical quantum yield of PSII (Fv/Fm) and nonphotochemical quenching (NPQ) were not affected by salt stress. However, Biyu was seriously affected under salt stress. Its growth indexes decreased by between 60 and 30% compared with the control and the photosynthetic indexes were also seriously affected under salt stress. This indicated that the salt-tolerant cultivar Qinghua improved the photosynthetic fluorescence ability to promote the synthesis of organic matter resulting in salt tolerance. In contrast, under alkali treatment, the root of Biyu was affected by alkali stress, but could still maintain good growth, and root and leaf structure were not seriously affected and could maintain the normal operations. Biyu improved its tolerance by improving the water use efficiency, regulating the synthesis of organic acids and carbohydrates, ensuring the synthesis of organic matter and ensured the normal growth of the plant.
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Abbreviations
- A:
-
Alkali stress
- C:
-
Control
- ETR:
-
Electron transfer rate of PSII
- Fv/Fm:
-
Maximum photochemical quantum yield of PSII
- Gs:
-
Stomatal conductance
- NPQ:
-
Non-photochemical quenching
- Pn:
-
Net photosynthetic rate
- SA:
-
Salt–alkali stress
- S:
-
Salt stress
- Tr:
-
Transpiration rate
- WUE:
-
Water use efficiency
References
Aisha S, Muntaz S, Raza S, Khan M, Solangi S (2005) Salinity effects on seeding growth and yield com ponents of different inbred rice lines. Pak J Bot 37(1):131–139
Baetz U, Martinoia E (2014) Root exudates: the hidden part of plant defense. Trends Plant Sci 19(2):90–98. https://doi.org/10.1016/j.tplants.2013.11.006
Caruso G (2008) Identification of changes in Triticum durum L. leaf proteome in response to salt stress by two-dimensional electrophoresis and maldi-tof mass spectrometry. Anal Bioanal Chem 391(1):381–390. https://doi.org/10.1007/s00216-008-2008-x
Flowers TJ (2004) Improving crop salt tolerance. J Exp Bot 55(396):307–319. https://doi.org/10.1093/jxb/erh003
Flowers TJ, Flowers SA (2005) Why does salinity pose such a difficult problem for plant breeders? Agric Water Manag 78(1):15–24. https://doi.org/10.1016/j.agwat.2005.04.015
Gao HJ, Yang HY, Bai JP, Liang XY, Lou Y, Zhang JL, Wang D, Zhang JL, Niu SQ, Chen YL (2014) Ultrastructural and physiological responses of potato (Solanum tuberosum L.) plantlets to gradient saline stress. Front Plant Sci 5:787. https://doi.org/10.3389/fpls.2014.00787
Gong B, Wen D, Bloszies S, Li X, Wei M, Yang F, Shi Q, Wang X (2014) Comparative effects of NaCl and NaHCO3 stresses on respiratory metabolism, antioxidant system, nutritional status, and organic acid metabolism in tomato roots. Acta Physiol Plant 36(8):2167–2181. https://doi.org/10.1007/s11738-014-1593-x
Gong B, Wen D, Wang X, Wei M, Yang F, Li Y, Shi Q (2015) S-nitrosoglutathione reductase-modulated redox signaling controls sodic alkaline stress responses in Solanum lycopersicum L. Plant Cell Physiol 56(4):790–802. https://doi.org/10.1093/pcp/pcv007
Goussi R, Manaa A, Derbali W, Cantamessa S, Abdelly C, Barbato R (2018) Comparative analysis of salt stress, duration and intensity, on the chloroplast ultrastructure and photosynthetic apparatus in Thellungiella salsuginea. J Photochem Photobiol B 183:275–287. https://doi.org/10.1016/j.jphotobiol.2018.04.047
Guntzer F, Keller C, Meunier J-D (2011) Benefits of plant silicon for crops: a review. Agron Sustain Dev 32(1):201–213. https://doi.org/10.1007/s13593-011-0039-8
Guo L (2009) Comparative study on regulation of organic acid metabolism in salt-alkali stress of Puccinellia tenuiflora. J North nor Univer 41(4):123–128
Guo R, Yang Z, Li F, Yan C, Zhong X, Liu Q, Xia X, Li H, Zhao L (2015) Comparative metabolic responses and adaptive strategies of wheat (Triticum aestivum) to salt and alkali stress. BMC Plant Biol 15:170. https://doi.org/10.1186/s12870-015-0546-x
Hunsche M, Lankes C, Hoffstall H, Noga G (2010) Vegetative performance, leaf water potential, and partitioning of minerals and soluble sugars: Traits for ranking the NaCl-tolerance of tomato genotypes? Plant Growth Regul 62(2):151–162. https://doi.org/10.1007/s10725-010-9500-y
Jia X, Wang H, Sofkova S, Yanfang Zhu HuY, Cheng L, Zhao T, Wang Y (2019) Comparative physiological responses and adaptive strategies of apple Malus halliana to salt, alkali and saline-alkali stress. Sci Hortic 245:154–162. https://doi.org/10.1016/j.scienta.2018.10.017
Kirchhoff H (2019) Chloroplast ultrastructure in plants. New Phytol 223(2):565–574. https://doi.org/10.1111/nph.15730
Kramer DM, Johnson G, Kiirats O, Edwards GE (2004) New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynth Res 79:209–218
Li T, Heuvelink E, Dueck TA, Janse J, Gort G, Marcelis LF (2014) Enhancement of crop photosynthesis by diffuse light: quantifying the contributing factors. Ann Bot 114(1):145–156. https://doi.org/10.1093/aob/mcu071
Li M, Petrie MD, Tariq A, Zeng F (2021a) Response of nodulation, nitrogen fixation to salt stress in a desert legume Alhagi sparsifolia. Environ Exp Bot. https://doi.org/10.1016/j.envexpbot.2020.104348
Li N, Zhang Z, Chen Z, Cao B, Xu K (2021b) Comparative transcriptome analysis of two contrasting Chinese cabbage (Brassica rapa L.) genotypes reveals that ion homeostasis is a crucial biological pathway involved in the rapid adaptive response to salt stress. Front Plant Sci 12:683891. https://doi.org/10.3389/fpls.2021.683891
Liu J, Shi D (2010) Photosynthesis, chlorophyll fluorescence, inorganic ion and organic acid accumulations of sunflower in responses to salt and salt-alkaline mixed stress. Photosynthetica 48(1):127–134
Liu XZ, Wang CZ, Su Q (2013) Screening for salt tolerance in eight halophyte species from Yellow River Delta at the two initial growth stages. ISRN Agron 2013:1–8. https://doi.org/10.1155/2013/592820
Ma H, Meng C, Zhang K, Wang K, Fan H, Li Y (2020) Study on physiological mechanism of using cottonseed meal to improve salt–alkali tolerance of cotton. J Plant Growth Regul 1(1):1–11. https://doi.org/10.1007/s00344-020-10083-7
Maeda Y, Nagasawa T, Tsurumi T, Iida K, Nakazawa R, Tadano T (2011) Physiological characteristics of salt tolerance in centipedegrass (Eremochloa ophiuroides (Munro) Hack. cv. TifBlair). Grassl Sci 57(2):65–71. https://doi.org/10.1111/j.1744-697X.2011.00210.x
Manivannan P, Jaleel CA, Sankar B, Kishorekumar A, Murali PV, Somasundaram R, Panneerselvam R (2008) Mineral uptake and biochemical changes in Helianthus annuus under treatment with different sodium salts. Colloids Surf B Biointerfaces 62(1):58–63. https://doi.org/10.1016/j.colsurfb.2007.09.019
Mehta P, Jajoo A, Mathur S, Bharti S (2010) Chlorophyll a fluorescence study revealing effects of high salt stress on photosystem II in wheat leaves. Plant Physiol Biochem 48(1):16–20. https://doi.org/10.1016/j.plaphy.2009.10.006
Mittal S, Kumari N, Sharma V (2012) Differential response of salt stress on Brassica juncea: photosynthetic performance, pigment, proline, D1 and antioxidant enzymes. Plant Physiol Biochem 54:17–26. https://doi.org/10.1016/j.plaphy.2012.02.003
Morant-Manceau A, Pradier E, Tremblin G (2004) Osmotic adjustment, gas exchanges and chlorophyll fluorescence of a hexaploid Triticale and its parental species under salt stress. J Plant Physiol 161(1):25–33. https://doi.org/10.1078/0176-1617-00963
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681. https://doi.org/10.1146/annurev.arplant.59.032607.092911
Naeem MS, Warusawitharana H, Liu H, Liu D, Ahmad R, Waraich EA, Xu L, Zhou W (2012) Aminolevulinic acid alleviates the salinity-induced changes in Brassica napus as revealed by the ultrastructural study of chloroplast. Plant Physiol Biochem 57:84–92. https://doi.org/10.1016/j.plaphy.2012.05.018
Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60(3):324–349. https://doi.org/10.1016/j.ecoenv.2004.06.010
Peharec Stefanic P, Koffler T (2013) Chloroplasts of salt-grown Arabidopsis seedlings are impaired in structure, genome copy number and transcript levels. PLoS ONE 8(12):e82548. https://doi.org/10.1371/journal.pone.0082548
Prechtl RM, Wefers D, Jakob F, Vogel RF (2018) Cold and salt stress modulate amount, molecular and macromolecular structure of a Lactobacillus sakei dextran. Food Hydrocoll 82:73–81. https://doi.org/10.1016/j.foodhyd.2018.04.003
Rivero RM, Mestre TC, Mittler R, Rubio F, Garcia-Sanchez F, Martinez V (2014) The combined effect of salinity and heat reveals a specific physiological, biochemical and molecular response in tomato plants. Plant Cell Environ 37(5):1059–1073. https://doi.org/10.1111/pce.12199
Roy SJ, Negrao S, Tester M (2014) Salt resistant crop plants. Curr Opin Biotechnol 26:115–124. https://doi.org/10.1016/j.copbio.2013.12.004
Said-Al Ahl HAH, Meawad AA, Abou-Zeid EN, Ali MS (2010) Response of different basil varieties to soil salinity. Int Agrophys 24:183–188
Schreiber U (1983) Chlorophyll fluorescence yield changes as a tool in plant physiology I. The measuring system. Photosynth Res 4(1):361–373
Shahbaz M, Ashraf M (2013) Improving salinity tolerance in cereals. CRC Crit Rev Plant Sci 32(4):237–249. https://doi.org/10.1080/07352689.2013.758544
Shi D, Li Y, Guo H, Li Y, Zhao K (2002) Artificial simulation of saline-alkali mixed ecological condition and analysis of stress factors on Leymus chinensis. Acta Ecol Sin 22(8):1323–1332
Soares ALC, Geilfus CM, Carpentier SC (2018) Genotype-specific growth and proteomic responses of maize toward salt stress. Front Plant Sci 9:661. https://doi.org/10.3389/fpls.2018.00661
Trotta A, Redondo Gomez S, Pagliano C, Clemente ME, Rascio N, La Rocca N, Antonacci A, Andreucci F, Barbato R (2012) Chloroplast ultrastructure and thylakoid polypeptide composition are affected by different salt concentrations in the halophytic plant Arthrocnemum macrostachyum. J Plant Physiol 169(2):111–116. https://doi.org/10.1016/j.jplph.2011.11.001
Turan MA, Hassan A, Elkarim A, Taban N, Taban S (2009) Effect of salt stress on growth, stomatal resistance, proline and chlorophyll concentrations on maize plant. Afr J Agric Res 4(9):893–897
Walter A, Rascher U, Osmond B (2004) Transitions in photosynthetic parameters of midvein and interveinal regions of leaves and their importance during leaf growth and development. Plant Biol (stuttg) 6(2):184–191. https://doi.org/10.1055/s-2004-817828
Wan C, Cui P, Sun H, Guo W, Yang C, Jin H, Fang B, Shi D (2009) Comparative effects of salt and alkali stresses on organic acid accumulation and ionic balance of seabuckthorn (Hippophae rhamnoides L.). Ind Crops Prod 30(3):351–358. https://doi.org/10.1016/j.indcrop.2009.06.007
Wei H, Bausewein A, Greiner S, Dauchot N, Harms K, Rausch T (2017a) CiMYB17, a stress-induced chicory R2R3-MYB transcription factor, activates promoters of genes involved in fructan synthesis and degradation. New Phytol 215(1):281–298. https://doi.org/10.1111/nph.14563
Wei Y, Xu Y, Lu P, Wang X, Li Z, Cai X, Zhou Z, Wang Y, Zhang Z, Lin Z, Liu F, Wang K (2017b) Salt stress responsiveness of a wild cotton species (Gossypium klotzschianum) based on transcriptomic analysis. PLoS ONE 12(5):e0178313. https://doi.org/10.1371/journal.pone.0178313
Yamori W (2016) Photosynthetic response to fluctuating environments and photoprotective strategies under abiotic stress. J Plant Res 129(3):379–395. https://doi.org/10.1007/s10265-016-0816-1
Yan Y, Jing X, Tang H, Li X, Gong B, Shi Q (2019) Using transcriptome to discover a novel melatonin-induced ssodic alkaline stress resistant pathway in Solanum lycopersicum L. Plant Cell Physiol 60(9):2051–2064. https://doi.org/10.1093/pcp/pcz126
Yan G, Fan X, Zheng W, Gao Z, Yin C, Li T, Liang Y (2021) Silicon alleviates salt stress-induced potassium deficiency by promoting potassium uptake and translocation in rice (Oryza sativa L.). J Plant Physiol 258–259:153379. https://doi.org/10.1016/j.jplph.2021.153379
Yang C, Chong J, Li C, Kim C, Shi D, Wang D (2007) Osmotic adjustment and ion balance traits of an alkali resistant halophyte Kochia sieversiana during adaptation to salt and alkali conditions. Plant Soil 294(1):263–276. https://doi.org/10.1007/s11104-007-9251-3
Yang C, Shi D, Wang D (2008) Comparative effects of salt and alkali stresses on growth, osmotic adjustment and ionic balance of an alkali-resistant halophyte Suaeda glauca (Bge.). Plant Growth Regul 56(2):179–190. https://doi.org/10.1007/s10725-008-9299-y
Yang C, Xu H, Wang L, Liu J, Shi D, Wang D (2009) Comparative effects of salt-stress and alkali-stress on the growth, photosynthesis, solute accumulation, and ion balance of barley plants. Photosynthetica 47(1):79–86
Yu NI, Lee SA, Lee MH, Heo JO, Chang KS, Lim J (2010) Characterization of SHORT-ROOT function in the Arabidopsis root vascular system. Mol Cells 30(2):113–119. https://doi.org/10.1007/s10059-010-0095-y
Zeng WH, Cheng BZ, Peng Y, Li Z (2019) Effects on germination and seeding drought tolerance in white clover of seed soaking with mannose. Acta Pratacul Sin 28(7):112–122 (in Chinese)
Zhang X, Lu G, Long W, Zou X, Li F, Nishio T (2014) Recent progress in drought and salt tolerance studies in Brassica crops. Breed Sci 64(1):60–73. https://doi.org/10.1270/jsbbs.64.60
Zhang K, Wen T, Dong J, Ma F, Bai T, Wang K, Li C (2016a) Comprehensive evaluation of tolerance to alkali stress by 17 genotypes of apple rootstocks. J Integr Agric 15(7):1499–1509. https://doi.org/10.1016/s2095-3119(15)61325-9
Zhang Y, Ma H, Calderón Urrea A, Tian C, Bai X, Wei J (2016b) Anatomical changes to protect organelle integrity account for tolerance to alkali and salt stresses in Melilotus officinalis. Plant Soil 406(1):327–340. https://doi.org/10.1007/s11104-016-2875-4
Zhang Q, Liu NF, Xiang ZX, Yang ZJ, Jiang YL, Hu LX (2017) Effects of neutral and alkaline salt stresses on the growth and physiological metabolism of Kentucky bluegrass. Acta Pratacul Sin 26(12):67–76 ((in chinese))
Zhao K, Zhou BH, Ma WZ, Yang LM (2016) The influence of different environmental stresses on root-exuded organic acids: a review. Soils 48(2):235–240. https://doi.org/10.13758/j.cnki.tr.2016.02.004 ((in chinese))
Zuo Z, Chen Z, Zhu Y, Bai Y, Wang Y (2014) Effects of NaCl and Na2CO3 stresses on photosynthetic ability of Chlamydomonas reinhardtii. Biol Plant. https://doi.org/10.2478/s11756-014-0437-x
Acknowledgements
We acknowledge all the members of the research team for their assistance in the field and laboratory work. We acknowledge the support of the Shandong Province’s dual class discipline construction project (Grant No. SYL2017YSTD06), the Agricultural application technology innovation project in Shandong Province of China (Grant No. 310131), and the China Agriculture Research System (Grant No. CARS-24-A-09).
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425_2021_3754_MOESM1_ESM.tif
Supplementary file1 (TIF 2517 KB) Fig. S1 Effects of salt and alkali stress on the root anatomical structure of Chinese Cabbage. Control (C), exposed to salt stress (S), alkali stress (A) and salt–alkali stress (SA). Endodermal cell (ec), phloem (p), xylem (x)
425_2021_3754_MOESM2_ESM.tif
Supplementary file2 (TIF 153 KB) Fig. S2 Vascular column area of the root anatomical structure of Chinese cabbage under salt stress and alkali stress. Control (C), salt stress (S), alkali stress (A) and salt–alkali stress (SA)
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Li, N., Zhang, Z., Gao, S. et al. Different responses of two Chinese cabbage (Brassica rapa L. ssp. pekinensis) cultivars in photosynthetic characteristics and chloroplast ultrastructure to salt and alkali stress. Planta 254, 102 (2021). https://doi.org/10.1007/s00425-021-03754-6
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DOI: https://doi.org/10.1007/s00425-021-03754-6