Abstract
In order to investigate the salt stress induced chlorophyll biosynthesis-related genes in photoheterotrophic cultures, we performed RNA-Seq analysis on A. thaliana calli exposed to 100 mM NaCl on MS medium containing 0.5 mg/L 2,4-D 30 days. Four different conditions of samples were sequenced on Illumina HiSeq Platform in total and generated about 4.49 Gb per sample. The average genome and gene map** rates were 93.52% and 90.78%, respectively. According to expression profile analysis, some DEGs demonstrated altered related to chlorophyll pigment metabolism. According to analysis, green callus color of photoheterotrophic calli were mainly connected with the induction of LHCB4.3 light harvesting complex photosystem II (Gene ID:818599), AT1G49975 photosystem I reaction center subunit N (Gene ID: 841421), PAM68 PAM68-like protein (DUF3464) (Gene ID: 2745715) and AT3G63540 thylakoid lumenal protein (Mog1/PsbP/DUF1795-like photosystem II reaction center PsbP family protein)(Gene ID: 7922413) genes. Furthermore, 8 DEGs were randomly selected to validate the transcriptome profiles via qPCR. These results will provide a foundation for further studies aimed at giving photosynthetic properties to in vitro plant cultures.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All data generated or analyzed during this study are included in this published article and its supplementary information files. The sequencing data were deposited in NCBI GEO under accession number GSE188818.
References
Amirjani MR (2011) Effect of salinity stress on growth, sugar content, pigments and enzyme activity of rice. Int J Botany 7: 73–81. https://scialert.net/abstract/?doi=ijb.2011.73.81
Arıkan B, Özden S, Turgut-Kara N (2018) DNA methylation related gene expression and morphophysiological response to abiotic stresses in Arabidopsis thaliana. Environ Exp Bot 149:17–26. https://doi.org/10.1016/j.envexpbot.2018.01.011
Armbruster U, Zühlke J, Rengstl B, Kreller R, Makarenko E, Rühle T, Schünemann D, Jahns P, Weisshaar B, Nickelsen J, Leister D (2010) The Arabidopsis thylakoid protein PAM68 is required for efficient D1 biogenesis and photosystem II assembly. Plant Cell 22(10):3439–60. https://doi.org/10.1105/tpc.110.077453
Ben-Amar A, Daldoul S, Allel D et al (2023) Ectopic expression of a grapevine alkaline α-galactosidase seed imbibition protein VvSIP enhanced salinity tolerance in transgenic tobacco plants. Funct Integr Genomics 23:12. https://doi.org/10.1007/s10142-022-00945-6
Bhatia S, Sharma K, Dahiya R, Bera T (2015) Plant tissue culture. In: Bhatia S, Sharma K, Dahiya R, Bera T (ed) Modern applications of plant biotechnology in pharmaceutical sciences Academic Press, Elsevier 31–107. https://doi.org/10.1016/C2014-0-02123-5
Breś W, Kleiber T, Markiewicz B, Mieloszyk E, Mieloch M (2022) The effect of NaCl stress on the response of lettuce (Lactuca sativa L.). Agron 12(2):244. https://doi.org/10.3390/agronomy12020244
Chen M, Telfer A, Lin S, Pascal A, Larkum AW, Barber J, Blankenship RE (2005) The nature of the photosystem II reaction center in the chlorophyll d-containing prokaryote. Acaryochloris Marina Photochem Photobiol Sci 4(12):1060–1064. https://doi.org/10.1039/B507057K
Chinnusamy V, Schumaker K, Zhu JK (2004) Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants. J Exp Bot 55(395):225–236. https://doi.org/10.1093/jxb/erh00
Chutipaijit S, Cha-um S, Sompornpailin K (2011) High contents of proline and anthocyanin increase protective response to salinity in “Oryza sativa” L. spp. “indica.” Aust J Crop Sci 5(10):1191–1198. https://doi.org/10.3316/informit.746208527906618
Das P, Majumder AL (2019) Transcriptome analysis of grapevine under salinity and identification of key genes responsible for salt tolerance. Funct Integr Genomics 19:61–73. https://doi.org/10.1007/s10142-018-0628-6
de Bianchi S, Betterle N, Kouril R, Cazzaniga S, Boekema E, Bassi R, Dall’Osto L (2011) Arabidopsis mutants deleted in the light-harvesting protein Lhcb4 have a disrupted photosystem II macrostructure and are defective in photoprotection. Plant Cell 23(7):2659–2679. https://doi.org/10.1105/tpc.111.087320
Dong P, **ong F, Que Y, Wang K, Yu L, Li Z, Maozhi R (2015) Expression profiling and functional analysis reveals that TOR is a key player in regulating photosynthesis and phytohormone signaling pathways in Arabidopsis. Front Plant Sci 6:677. https://doi.org/10.3389/fpls.2015.00677
Dong S, Sang L, **e H, Chai M, Wang Z-Y (2021) Comparative Transcriptome Analysis of Salt Stress-Induced Leaf Senescence in Medicago truncatula. Front Plant Sci 12:666660. https://doi.org/10.3389/fpls.2021.666660
Eckhardt U, Grimm B, Hörtensteiner S (2004) Recent advances in chlorophyll biosynthesis and breakdown in higher plants. Plant Mol Biol 1:1–14. https://doi.org/10.1007/s11103-004-2331-3
Frank W, Ratnadewi D, Reski R (2005) Physcomitrella patens is highly tolerant against drought, salt and osmotic stress. Planta 220:384–394. https://doi.org/10.1007/s00425-004-1351-1
Geilfus CM (2019) Light. In: Controlled Environment Horticulture. Springer, Cham. https://doi.org/10.1007/978-3-030-23197-2_5
Gupta AS, Berkowitz GA (1988) Chloroplast osmotic adjustment and water stress effects on photosynthesis. Plant Physiol 88(1):200–206. https://doi.org/10.1104/pp.88.1.200
Haldrup A, Naver H, Scheller HV (1999) The interaction between plastocyanin and photosystem I is inefficient in transgenic Arabidopsis plants lacking the PSI-N subunit of photosystem. Plant J 17(6):689–698. https://doi.org/10.1046/j.1365-313X.1999.00419.x
Harvey A, Edrada-Ebel R, Quinn R (2015) The re-emergence of natural products for drug discovery in the genomics era. Nat Rev Drug Discov 14:111–129. https://doi.org/10.1038/nrd4510
Ihalainen JA, Jensen PE, Haldrup A, van Stokkum IH, van Grondelle R, Scheller HV, Dekker JP (2002) Pigment organization and energy transfer dynamics in isolated photosystem I (PSI) complexes from Arabidopsis thaliana depleted of the PSI-G, PSI-K, PSI-L, or PSI-N subunit. Biophys J 83(4):2190–2201. https://doi.org/10.1016/S0006-3495(02)73979-9
Islam F, Farooq MA, Gill RA et al (2017) 2,4-D attenuates salinity-induced toxicity by mediating anatomical changes, antioxidant capacity and cation transporters in the roots of rice cultivars. Sci Rep 7:10443. https://doi.org/10.1038/s41598-017-09708-x
Jung KH, Hur J, Ryu CH, Choi Y, Chung YY, Miyao A et al (2003) Characterization of a rice chlorophyll-deficient mutant using the T-DNA gene-trap system. Plant Cell Physiol 44(5):463–472. https://doi.org/10.1093/pcp/pcg064
Kalaji MH, Govindjee BK, Kościelniak J, Żuk-Gołaszewska K (2011) Effects of salt stress on photosystem II efficiency and CO2 assimilation of two Syrian barley landraces. Environ Exp Bot 73:64–72. https://doi.org/10.1016/j.envexpbot.2010.10.009
Kato Y, Miura E, Matsushima R, Sakamoto W (2007) White leaf sectors in yellow variegated2 are formed by viable cells with undifferentiated plastids. Plant Physiol 144:952–960. https://doi.org/10.1104/pp.107.099002
Khan MM, Al-Mas'oudi RSM, Al-Said F, Khan I (2013) Salinity effects on growth, electrolyte leakage, chlorophyll content and lipid peroxidation in cucumber (Cucumis sativus L.). International Conference on Food and Agricultural Sciences IPCBEE 55:28–32, IACSIT Press, Singapore. https://doi.org/10.7763/IPCBEE
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25(4):402–408. https://doi.org/10.1006/meth.2001.1262
Lòpez-Climent MF, Arbona V, Pérez-Clemente RM, Gòmez-Cadenas A (2008) Relationship between salt tolerance and photosynthetic machinery performance in citrus. Environ Exp Bot 62:176–184. https://doi.org/10.1016/j.envexpbot.2007.08.002
Lu Y (2016) Identification and roles of photosystem ii assembly, stability, and repair factors in Arabidopsis. Front Plant Sci 7:168. https://doi.org/10.3389/fpls.2016.00168
Mane AV, Karadge BA, Samant JS (2010) Salinity induced changes in photosynthetic pigments and polyphenols of Cymbopogon nardus (L.) Rendle. J Chem Pharm Res 2(3):338–347
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
Motohashi R, Ito T, Kobayashi M, Taji T, Nagata N, Asami T et al (2003) Functional analysis of the 37 kDa inner envelope membrane polypeptide in chloroplast biogenesis using a Ds-tagged Arabidopsis pale-green mutant. Plant J 34(5):719–731. https://doi.org/10.1046/j.1365-313X.2003.01763.x
Munns R (2005) Genes and Salt Tolerance; Bringing Them Together. New Phytol 167:645–663. https://doi.org/10.1111/j.1469-8137.2005.01487.x
Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15(3):473–497
Ogbonna J, Ichige E, Tanaka H (2002) Interactions between photoautotrophic and heterotrophic metabolism in photoheterotrophic cultures of Euglena gracilis. Appl Microbiol Biotechnol 58:532–538. https://doi.org/10.1007/s00253-001-0901-8
Pinto AÁF (2016) 2, 4-dichlorophenoxy acetic acid-mediated stress in tomato plants: a biochemical and molecular approach. Dissertation, Department of Biology, Universidade de Porto, Portugal
Šamec D, Lini CI, Salopek-Sondi B (2021) Salinity stress as an elicitor for phytochemicals and minerals accumulation in selected leafy vegetables of Brassicaceae. Agron 11:361. https://doi.org/10.3390/agronomy11020361
Sankari M, Hridya H, Sneha P et al (2019) Implication of salt stress induces changes in pigment production, antioxidant enzyme activity, and qRT-PCR expression of genes involved in the biosynthetic pathway of Bixa orellana L. Funct Integr Genomics 19:565–574. https://doi.org/10.1007/s10142-019-00654-7
Schuenemann D, Gupta S, Persello-Cartieaux F, Klimyuk VI, Jones JD, Nussaume L, Hoffman NE (1998) A novel signal recognition particle targets light-harvesting proteins to the thylakoid membranes. Proc Natl Acad Sci USA 95(17):10312–10316. https://doi.org/10.1073/pnas.95.17.10312
Sudhir P, Murthy SDS (2004) Effects of salt stress on basic processes of photosynthesis. Photosynthetica 42(4):481–486. https://doi.org/10.1007/S11099-005-0001-6
Taïbi K, Taïbi F, Abderrahim LA, Ennajah A, Belkhodja M, Mulet JM (2016) Effect of salt stress on growth, chlorophyll content, lipid peroxidation and antioxidant defence systems in Phaseolus vulgaris L. S Afr J Bot 105:306–312. https://doi.org/10.1016/j.sajb.2016.03.011
Teramoto H, Nakamori A, Minagawa J, Ono TA (2002) Light-intensity-dependent expression of LHC gene family encoding light-harvesting chlorophyll-a/b proteins of photosystem II in Chlamydomonas reinhardtii. Plant Physiol 130:325–333. https://doi.org/10.1104/pp.004622
Tsugane K, Kobayashi K, Niwa Y, Ohba Y, Wada K, Kobayashi H (1999) A recessive Arabidopsis mutant that grows photoautotrophically under salt stress shows enhanced active oxygen detoxification. Plant Cell 11(7):1195–1206. https://doi.org/10.1105/tpc.11.7.1195
Wang H, Liang X, Wan Q et al (2009) Ethylene and nitric oxide are involved in maintaining ion homeostasis in Arabidopsis callus under salt stress. Planta 230:293–307. https://doi.org/10.1007/s00425-009-0946-y
Wiedemann G, Koprivova A, Schneider M, Herschbach C, Reski R, Kopriva S (2007) The role of the novel adenosine 50-phosphosulfate reductase in regulation of sulfate assimilation of Physcomitrella patens. Plant Mol Biol 65(5):667–676. https://doi.org/10.1007/s11103-007-9231-2
Wong PK (2000) Effects of 2, 4-D, glyphosate and paraquat on growth, photosynthesis and chlorophyll–a synthesis of Scenedesmus quadricauda Berb 614. Chemosphere 41(1–2):177–182. https://doi.org/10.1016/S0045-6535(99)00408-7
Zhao X, Tan HJ, Liu YB et al (2009) Effect of salt stress on growth and osmotic regulation in Thellungiella and Arabidopsis callus. Plant Cell Tiss Org 98:97–103. https://doi.org/10.1007/s11240-009-9542-x
Funding
The authors gratefully acknowledge financial support of Istanbul University Scientific Research Project Coordination Unit with project no: 22633.
Author information
Authors and Affiliations
Contributions
HÇ, BA, CU and NTK conceived and designed the research. All authors conducted the experiments and analyzed the data. ÖÇ, NTK and BA wrote the manuscript, and all authors read and approved the manuscript.
Corresponding author
Ethics declarations
Ethical approval
Not applicable.
Competing interests
The authors declare that they have no known competing financial or personal interests.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Çelik, H., Arıkan, B., Kara, N.T. et al. Transcriptomic analysis of salt stress induced chlorophyll biosynthesis-related genes in photoheterotrophic Arabidopsis thaliana calli. Funct Integr Genomics 23, 146 (2023). https://doi.org/10.1007/s10142-023-01076-2
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10142-023-01076-2