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Screening of salt stress in the overexpressed type of Arabidopsis thaliana (L.) Heynh. for the identification of significant hub genes using a systems biology approach

DOI
https://doi.org/10.14719/pst.1301
Submitted
7 June 2021
Published
23-07-2022
Versions

Abstract

Worldwide, it is known that abiotic and biotic stresses can affect the production of crops by a declining trend. To control the situation, SnRK2 (a subfamily 2 of SNF1-related protein kinase) overexpression levels can induce salt tolerance. This study used a dataset for 2 types of Arabidopsis thaliana including the wild and PtSnRK2.7 overexpressed in mock and salt conditions to compare and identify the salt stress-responsive genes. A computational systems biology approach was employed to identify the differentially expressed genes and determine their mechanisms in terms of molecular functionalities, cellular components, KEGG enrichment pathways and plant ontology analyses. The results indicate that the 15 genes identified for PtSnRK2.7 overexpressed type in mock against salt conditions were upregulated (AT1G19180 and AT2G23150 were downregulated) and related to various environmental stresses. Furthermore, 8 out of 15 identified genes were downregulated for the wild type exposed to salt stress and the rest were upregulated. And, the only upregulated gene found differentially expressed between wild and overexpressed types in salt stress conditions was AT4G15110. In contrast, the other two AT1G15010 and AT4G19430 were downregulated and involved in transient stress and inactivation of chloroplast, respectively. Taken together, it has been shown that A. thaliana PtSnRK2.7 overexpressed type can resist salt stress. Finally, more experimental studies and computational systems biology methodologies are needed to reveal and confirm the responsive gene for salt stress in A. thaliana.

References

  1. Yadav SP, Bharadwaj R, Nayak H, Mahto R, Singh RK, Prasad SK. Impact of salt stress on growth, productivity and physicochemical properties of plants: A Review. IJCS. 2019;7(2):1793-98.
  2. Yamaguchi T, Blumwald E. Developing salt-tolerant crop plants: challenges and opportunities. Trends in Plant Science. 2005;10(12):615-20.https://doi.org/10.1016/j.tplants.2005.10.002
  3. Morton MJ, Awlia M, Al?Tamimi N, Saade S, Pailles Y, Negrão S et al. Salt stress under the scalpel-dissecting the genetics of salt tolerance. The Plant Journal. 2019;97(1):148-63.https://doi.org/10.1111/tpj.14189
  4. Acosta-Motos JR, Ortuño MF, Bernal-Vicente A, Diaz-Vivancos P, Sanchez-Blanco MJ, Hernandez JA. Plant Responses to Salt Stress: Adaptive Mechanisms. Agronomy. 2017;7(1):18. https://doi.org/10.3390/agronomy7010018
  5. Pardo JM. Biotechnology of water and salinity stress tolerance. Current Opinion in Biotechnology. 2010;21(2):185-96. https://doi.org/10.1016/j.copbio.2010.02.005
  6. Evelin H, Devi TS, Gupta S, Kapoor R. Mitigation of salinity stress in plants by arbuscular mycorrhizal symbiosis: current understanding and new challenges. Frontiers in Plant Science. 2019;10:470. https://doi.org/10.3389/fpls.2019.00470
  7. Islam F, Wang J, Farooq MA, Yang C, Jan M, Mwamba TM et al. Rice responses and tolerance to salt stress: Deciphering the physiological and molecular mechanisms of salinity adaptation. Advances in Rice Research for Abiotic Stress Tolerance: Elsevier; 2019. p. 791-819. https://doi.org/10.1016/B978-0-12-814332-2.00040-X
  8. Prasad B, Karodia S, Malviya J. Identifying genes responsible for shoot development in Arabidopsis thaliana using microarray technique. Research Journal of Life Sciences, Bioinformatics, Pharmaceutical and Chemical Sciences. 2019;5(1):262-82.
  9. Meinke DW, Cherry JM, Dean C, Rounsley SD, Koornneef M. Arabidopsis thaliana: a model plant for genome analysis. Science. 1998;282(5389):662-82. https://doi.org/10.1126/science.282.5389.662
  10. Liu H-H, Tian X, Li Y-J, Wu C-A, Zheng C-C. Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana. Rna. 2008;14(5):836-43. https://doi.org/10.1261/rna.895308
  11. Patankar HV, Al-Harrasi I, Al Kharusi L, Jana GA, Al-Yahyai R, Sunkar R et al. Overexpression of a metallothionein 2A gene from date palm confers abiotic stress tolerance to yeast and Arabidopsis thaliana. International Journal of Molecular Sciences. 2019;20(12):2871. https://doi.org/10.3390/ijms20122871
  12. Coolen S, Van Pelt JA, Van Wees SC, Pieterse CM. Mining the natural genetic variation in Arabidopsis thaliana for adaptation to sequential abiotic and biotic stresses. Planta. 2019;249(4):1087-105.https://doi.org/10.1007/s00425-018-3065-9
  13. Kulik A, Wawer I, Krzywi?ska E, Bucholc M, Dobrowolska G. SnRK2 protein kinases-key regulators of plant response to abiotic stresses. Omics: a Journal of Integrative Biology. 2011;15(12):859-72.https://doi.org/10.1089/omi.2011.0091
  14. Liu Z, Ge X, Yang Z, Zhang C, Zhao G, Chen E et al. Genome-wide identification and characterization of SnRK2 gene family in cotton (Gossypium hirsutum L.). BMC Genetics. 2017;18(1):54. https://doi.org/10.1186/s12863-017-0517-3
  15. Song X, Yu X, Hori C, Demura T, Ohtani M, Zhuge Q. Heterologous overexpression of poplar SnRK2 genes enhanced salt stress tolerance in Arabidopsis thaliana. Frontiers in Plant Science. 2016;7:612. https://doi.org/10.3389/fpls.2016.00612
  16. Carlson M. ath1121501.db: Affymetrix Arabidopsis ATH1 Genome Array annotation data (chip ath1121501). Bioconductororg. 2016.
  17. Yi X, Du Z, Su Z. PlantGSEA: a gene set enrichment analysis toolkit for plant community. Nucleic Acids Research. 2013;41(W1):W98-W103.https://doi.org/10.1093/nar/gkt281
  18. Nepusz T, Yu H, Paccanaro A. Detecting overlapping protein complexes in protein-protein interaction networks. Nature Methods. 2012;9(5):471-72. https://doi.org/10.1038/nmeth.1938
  19. Chin C-H, Chen S-H, Wu H-H, Ho C-W, Ko M-T, Lin C-Y. cytoHubba: identifying hub objects and sub-networks from complex interactome. BMC Syst Biol. 2014;8(4):S11.https://doi.org/10.1186/1752-0509-8-S4-S11
  20. Teshome DT, Zharare GE, Naidoo S. The threat of the combined effect of biotic and abiotic stress factors in forestry under a changing climate. Frontiers in Plant Science. 2020;11(1874):601009. https://doi.org/10.3389/fpls.2020.601009
  21. Zampieri M, Weissteiner CJ, Grizzetti B, Toreti A, van den Berg M, Dentener F. Estimating resilience of crop production systems: From theory to practice. ScTEn. 2020;735:139378. https://doi.org/10.1016/j.scitotenv.2020.139378
  22. Fahad S, Bajwa AA, Nazir U, Anjum SA, Farooq A, Zohaib A et al. Crop production under drought and heat stress: Plant responses and management options. Frontiers in Plant Science. 2017;8:1147. https://doi.org/10.3389/fpls.2017.01147
  23. Lee TA, Bailey-Serres J. Integrative analysis from the epigenome to translatome uncovers patterns of dominant nuclear regulation during transient stress. The Plant Cell. 2019;31(11):2573-95. https://doi.org/10.1105/tpc.19.00463
  24. Dal Bosco C, Lezhneva L, Biehl A, Leister D, Strotmann H, Wanner G, et al. Inactivation of the chloroplast ATP synthase ? subunit results in high non-photochemical fluorescence quenching and altered nuclear gene expression in Arabidopsis thaliana. Journal of Biological Chemistry. 2004;279(2):1060-69. https://doi.org/10.1074/jbc.M308435200
  25. Schuler MA, Werck-Reichhart D. Functional genomics of P450s. Annual Review of Plant Biology. 2003;54(1):629-67. https://doi.org/10.1146/annurev.arplant.54.031902.134840
  26. Kim K, Yadav D, Cho M. Multi-phased internalization of murine norovirus (MNV) in Arabidopsis seedlings and its potential correlation with plant defensive responses. Microbial Pathogenesis. 2019;135:103648. https://doi.org/10.1016/j.micpath.2019.103648
  27. Ge Y, Sealfon SC, Speed TP. Multiple testing and its applications to microarrays. Stat Methods Med Res. 2009;18(6):543-63.https://doi.org/10.1177/0962280209351899
  28. Zhao Y, Simon R. BRB-ArrayTools Data Archive for human cancer gene expression: a unique and efficient data sharing resource. Cancer Inform. 2008;6:9-15. https://doi.org/10.4137/CIN.S448
  29. Méteignier LV, Ghandour R, Meierhoff K, Zimmerman A, Chicher J, Baumberger N et al. The Arabidopsis mTERF-repeat MDA1 protein plays a dual function in transcription and stabilization of specific chloroplast transcripts within the psbE and ndhH operons. New Phytol. 2020;227(5):1376-91. https://doi.org/10.1111/nph.16625
  30. Reinholdt O, Schwab S, Zhang Y, Reichheld JP, Fernie AR, Hagemann M et al. Redox-Regulation of Photorespiration through Mitochondrial Thioredoxin o1. Plant Physiol. 2019;181(2):442-57. https://doi.org/10.1104/pp.19.00559
  31. Jin Y, Chen S, Fan X, Song H, Li X, Xu J et al. Diuron treatment reveals the different roles of two cyclic electron transfer pathways in photosystem II in Arabidopsis thaliana. Pestic Biochem Physiol. 2017;137:15-20. https://doi.org/10.1016/j.pestbp.2016.09.002
  32. Qian H, Tsuji T, Endo T, Sato F. PGR5 and NDH pathways in photosynthetic cyclic electron transfer respond differently to sublethal treatment with photosystem-interfering herbicides. J Agric Food Chem. 2014;62(18):4083-89. https://doi.org/10.1021/jf500143f
  33. Rawat R, Sandoval FJ, Wei Z, Winkler R, Roje S. An FMN hydrolase of the haloacid dehalogenase superfamily is active in plant chloroplasts. J Biol Chem. 2011;286(49):42091-98. https://doi.org/10.1074/jbc.M111.260885
  34. Ehlting J, Sauveplane V, Olry A, Ginglinger JF, Provart NJ, Werck-Reichhart D. An extensive (co-)expression analysis tool for the cytochrome P450 superfamily in Arabidopsis thaliana. BMC Plant Biol. 2008;8:47. https://doi.org/10.1186/1471-2229-8-47
  35. Ascencio-Ibanez JT, Sozzani R, Lee T-J, Chu T-M, Wolfinger RD, Cella R et al. Global analysis of Arabidopsis gene expression uncovers a complex array of changes impacting pathogen response and cell cycle during geminivirus infection. Plant Physiology. 2008;148(1):436-54. https://doi.org/10.1104/pp.108.121038
  36. Yoshida K, Hisabori T. Determining the Rate-Limiting Step for Light-Responsive Redox Regulation in Chloroplasts. Antioxidants (Basel). 2018;7(11). https://doi.org/10.3390/antiox7110153
  37. Simkin AJ, Lopez-Calcagno PE, Davey PA, Headland LR, Lawson T, Timm S et al. Simultaneous stimulation of sedoheptulose 1,7-bisphosphatase, fructose 1,6-bisphophate aldolase and the photorespiratory glycine decarboxylase-H protein increases CO(2) assimilation, vegetative biomass and seed yield in Arabidopsis. Plant Biotechnol J. 2017;15(7):805-16. https://doi.org/10.1111/pbi.12676
  38. Bach-Pages M, Homma F, Kourelis J, Kaschani F, Mohammed S, Kaiser M et al. Discovering the RNA-binding proteome of plant leaves with an improved RNA interactome capture method. Biomolecules. 2020;10(4). https://doi.org/10.3390/biom10040661
  39. Fares A, Rossignol M, Peltier JB. Proteomics investigation of endogenous S-nitrosylation in Arabidopsis. Biochem Biophys Res Commun. 2011;416(3-4):331-36.
  40. https://doi.org/10.1016/j.bbrc.2011.11.036
  41. Rocha J, Nitenberg M, Girard-Egrot A, Jouhet J, Maréchal E, Block MA et al. Do galactolipid synthases play a key role in the biogenesis of chloroplast membranes of higher plants? Front Plant Sci. 2018;9:126. https://doi.org/10.3389/fpls.2018.00126
  42. Botté CY, Deligny M, Roccia A, Bonneau AL, Saïdani N, Hardré H et al. Chemical inhibitors of monogalactosyldiacylglycerol synthases in Arabidopsis thaliana. Nat Chem Biol. 2011;7(11):834-42. https://doi.org/10.1038/nchembio.658
  43. Abercrombie JM, Halfhill MD, Ranjan P, Rao MR, Saxton AM, Yuan JS et al. Transcriptional responses of Arabidopsis thaliana plants to As (V) stress. BMC Plant Biol. 2008;8:87. https://doi.org/10.1186/1471-2229-8-87
  44. Giraud E, Ho LH, Clifton R, Carroll A, Estavillo G, Tan YF et al. The absence of alternative oxidase1a in Arabidopsis results in acute sensitivity to combined light and drought stress. Plant Physiol. 2008;147(2):595-610. https://doi.org/10.1104/pp.107.115121
  45. Sottosanto JB, Saranga Y, Blumwald E. Impact of AtNHX1, a vacuolar Na+/H+ antiporter, upon gene expression during short- and long-term salt stress in Arabidopsis thaliana. BMC Plant Biol. 2007;7:18. https://doi.org/10.1186/1471-2229-7-18
  46. Dombrecht B, Xue GP, Sprague SJ, Kirkegaard JA, Ross JJ, Reid JB et al. MYC2 differentially modulates diverse jasmonate-dependent functions in Arabidopsis. Plant Cell. 2007;19(7):2225-45. https://doi.org/10.1105/tpc.106.048017
  47. Tran LS, Nakashima K, Sakuma Y, Simpson SD, Fujita Y, Maruyama K et al. Isolation and functional analysis of Arabidopsis stress-inducible NAC transcription factors that bind to a drought-responsive cis-element in the early responsive to dehydration stress 1 promoter. Plant Cell. 2004;16(9):2481-98. https://doi.org/10.1105/tpc.104.022699
  48. Bharti P, Mahajan M, Vishwakarma AK, Bhardwaj J, Yadav SK. AtROS1 overexpression provides evidence for epigenetic regulation of genes encoding enzymes of flavonoid biosynthesis and antioxidant pathways during salt stress in transgenic tobacco. J Exp Bot. 2015;66(19):5959-69. https://doi.org/10.1093/jxb/erv304
  49. Mahmood K, Xu Z, El-Kereamy A, Casaretto JA, Rothstein SJ. The Arabidopsis transcription factor ANAC032 represses anthocyanin biosynthesis in response to high sucrose and oxidative and abiotic stresses. Front Plant Sci. 2016;7:1548. https://doi.org/10.3389/fpls.2016.01548
  50. Huang KC, Lin WC, Cheng WH. Salt hypersensitive mutant 9, a nucleolar APUM23 protein, is essential for salt sensitivity in association with the ABA signaling pathway in Arabidopsis. BMC Plant Biol. 2018;18(1):40. https://doi.org/10.1186/s12870-018-1255-z
  51. Wang L, Waters MT, Smith SM. Karrikin?KAI2 signalling provides Arabidopsis seeds with tolerance to abiotic stress and inhibits germination under conditions unfavourable to seedling establishment. New Phytologist. 2018;219(2):605-18. https://doi.org/10.1111/nph.15192
  52. Divi UK, Rahman T, Krishna P. Gene expression and functional analyses in brassinosteroid?mediated stress tolerance. Plant Biotechnol J. 2016;14(1):419-32. https://doi.org/10.1111/pbi.12396
  53. Turek I, Irving H, Gehring C. Dataset on interactors of the Arabidopsis thaliana Plant Natriuretic Peptide (AtPNP-A) determined by mass spectrometry. Data Brief. 2020;30:105606. https://doi.org/10.1016/j.dib.2020.105606
  54. Lee KP, Liu K, Kim EY, Medina-Puche L, Dong H, Duan J et al. Plant natriuretic peptide A and its putative receptor PNP-R2 antagonize salicylic acid-mediated signaling and cell death. Plant Cell. 2020;32(7):2237-50. https://doi.org/10.1105/tpc.20.00018
  55. Gandia-Herrero F, Lorenz A, Larson T, Graham IA, Bowles DJ, Rylott EL et al. Detoxification of the explosive 2,4,6-trinitrotoluene in Arabidopsis: discovery of bifunctional O- and C-glucosyltransferases. Plant J. 2008;56(6):963-74. https://doi.org/10.1111/j.1365-313X.2008.03653.x
  56. Ascencio-Ibáñez JT, Sozzani R, Lee TJ, Chu TM, Wolfinger RD, Cella R et al. Global analysis of Arabidopsis gene expression uncovers a complex array of changes impacting pathogen response and cell cycle during geminivirus infection. Plant Physiol. 2008;148(1):436-54. https://doi.org/10.1104/pp.108.121038
  57. Li B, Fang J, Singh RM, Zi H, Lv S, Liu R et al. Fatty acid desaturase 5 is required to induce autoimmune responses in gigantic chloroplast mutants of Arabidopsis. Plant Cell. 2020;32(10):3240-55. https://doi.org/10.1105/tpc.20.00016
  58. Liu F, Zhao Q, Jia Z, Song C, Huang Y, Ma H et al. N-3-oxo-octanoyl-homoserine lactone-mediated priming of resistance to Pseudomonas syringae requires the salicylic acid signaling pathway in Arabidopsis thaliana. BMC Plant Biol. 2020;20(1):38. https://doi.org/10.1186/s12870-019-2228-6
  59. Li LS, Ying J, Li E, Ma T, Li M, Gong LM et al. Arabidopsis CBP60b is a central transcriptional activator of immunity. Plant Physiol. 2021;186(3):1645-59. https://doi.org/10.1093/plphys/kiab164
  60. Lee TA, Bailey-Serres J. Integrative analysis from the epigenome to translatome uncovers patterns of dominant nuclear regulation during transient stress. Plant Cell. 2019;31(11):2573-95. https://doi.org/10.1105/tpc.19.00463
  61. Tian L, Musetti V, Kim J, Magallanes-Lundback M, DellaPenna D. The Arabidopsis LUT1 locus encodes a member of the cytochrome p450 family that is required for carotenoid epsilon-ring hydroxylation activity. Proc Natl Acad Sci U S A. 2004;101(1):402-27. https://doi.org/10.1073/pnas.2237237100
  62. Kim JE, Cheng KM, Craft NE, Hamberger B, Douglas CJ. Over-expression of Arabidopsis thaliana carotenoid hydroxylases individually and in combination with a beta-carotene ketolase provides insight into in vivo functions. Phytochemistry. 2010;71(2-3):168-78. https://doi.org/10.1016/j.phytochem.2009.10.011
  63. Ko JH, Yang SH, Han KH. Upregulation of an Arabidopsis RING-H2 gene, XERICO, confers drought tolerance through increased abscisic acid biosynthesis. Plant J. 2006;47(3):343-55. https://doi.org/10.1111/j.1365-313X.2006.02782.x
  64. Dal Bosco C, Lezhneva L, Biehl A, Leister D, Strotmann H, Wanner G et al. Inactivation of the chloroplast ATP synthase gamma subunit results in high non-photochemical fluorescence quenching and altered nuclear gene expression in Arabidopsis thaliana. J Biol Chem. 2004;279(2):1060-69. https://doi.org/10.1074/jbc.M308435200
  65. Zybailov B, Rutschow H, Friso G, Rudella A, Emanuelsson O, Sun Q et al. Sorting signals, N-terminal modifications and abundance of the chloroplast proteome. PloS One. 2008;3(4):e1994. https://doi.org/10.1371/journal.pone.0001994
  66. Wang Y, Zeng L, Xing D. ROS-mediated enhanced transcription of CYP38 promotes the plant tolerance to high light stress by suppressing GTPase activation of PsbO2. Frontiers in Plant Science. 2015;6:777. https://doi.org/10.3389/fpls.2015.00777
  67. Zheng X, Chen L, Li X. Arabidopsis and rice showed a distinct pattern in ZIPs genes expression profile in response to Cd stress. Botanical Studies. 2018;59(1):22. https://doi.org/10.1186/s40529-018-0238-6
  68. Huang K-C, Lin W-C, Cheng W-H. Salt hypersensitive mutant 9, a nucleolar APUM23 protein, is essential for salt sensitivity in association with the ABA signaling pathway in Arabidopsis. BMC Plant Biology. 2018;18(1):40. https://doi.org/10.1186/s12870-018-1255-z
  69. Ulm R, Revenkova E, di Sansebastiano G-P, Bechtold N, Paszkowski J. Mitogen-activated protein kinase phosphatase is required for genotoxic stress relief in Arabidopsis. Genes and Development. 2001;15(6):699-709. https://doi.org/10.1101/gad.192601
  70. Yao X, Cai Y, Yu D, Liang G. bHLH104 confers tolerance to cadmium stress in Arabidopsis thaliana. Journal of Integrative Plant Biology. 2018;60(8):691-702. https://doi.org/10.1111/jipb.12658
  71. Mittal S, Mallikarjuna MG, Rao AR, Jain PA, Dash PK, Thirunavukkarasu N. Comparative analysis of CDPK family in maize, arabidopsis, rice and sorghum revealed potential targets for drought tolerance improvement. Frontiers in Chemistry. 2017;5:115. https://doi.org/10.3389/fchem.2017.00115
  72. Beemster G, De Jaeger G, editors. A systems approach to understand cell cycle regulation during leaf development. 18th International Conference on Arabidopsis Research 2007.
  73. Sánchez-Corrionero Á, Sánchez-Vicente I, González-Pérez S, Corrales A, Krieger-Liszkay A, Lorenzo Ó et al. Singlet oxygen triggers chloroplast rupture and cell death in the zeaxanthin epoxidase defective mutant aba1 of Arabidopsis thaliana under high light stress. Journal of Plant Physiology. 2017;216:188-96. https://doi.org/10.1016/j.jplph.2017.06.009
  74. Ndamukong I, Jones DR, Lapko H, Divecha N, Avramova Z. Phosphatidylinositol 5-phosphate links dehydration stress to the activity of Arabidopsis trithorax-like factor ATX1. PLoS One. 2010;5(10):e13396. https://doi.org/10.1371/journal.pone.0013396
  75. He XJ, Mu RL, Cao WH, Zhang ZG, Zhang JS, Chen SY. AtNAC2, a transcription factor downstream of ethylene and auxin signaling pathways, is involved in salt stress response and lateral root development. The Plant Journal. 2005;44(6):903-16. https://doi.org/10.1111/j.1365-313X.2005.02575.x
  76. Ma S, Bohnert HJ. Integration of Arabidopsis thaliana stress-related transcript profiles, promoter structures and cell-specific expression. Genome Biology. 2007;8(4):R49. https://doi.org/10.1186/gb-2007-8-4-r49
  77. Kaye Y, Golani Y, Singer Y, Leshem Y, Cohen G, Ercetin M et al. Inositol polyphosphate 5-phosphatase7 regulates the production of reactive oxygen species and salt tolerance in Arabidopsis. Plant Physiology. 2011;157(1):229-41. https://doi.org/10.1104/pp.111.176883
  78. Abeysinghe JK, Lam KM, Ng DWK. Differential regulation and interaction of homoeologous WRKY 18 and WRKY 40 in Arabidopsis allotetraploids and biotic stress responses. The Plant Journal. 2019;97(2):352-67. https://doi.org/10.1111/tpj.14124
  79. Van Aken O, De Clercq I, Ivanova A, Law SR, Van Breusegem F, Millar AH et al. Mitochondrial and chloroplast stress responses are modulated in distinct touch and chemical inhibition phases. Plant Physiology. 2016;171(3):2150-65. https://doi.org/10.1104/pp.16.00273
  80. Renault H, El Amrani A, Berger A, Mouille G, Soubigou-taconnat L, Bouchereau A et al. ??Aminobutyric acid transaminase deficiency impairs central carbon metabolism and leads to cell wall defects during salt stress in Arabidopsis roots. Plant, Cell and Environment. 2013;36(5):1009-18. https://doi.org/10.1111/pce.12033
  81. Dong C-H, Hu X, Tang W, Zheng X, Kim YS, Lee B-h et al. A putative Arabidopsis nucleoporin, AtNUP160, is critical for RNA export and required for plant tolerance to cold stress. Molecular and Cellular Biology. 2006;26(24):9533-43. https://doi.org/10.1128/MCB.01063-06
  82. Stanley Kim H, Yu Y, Snesrud EC, Moy LP, Linford LD, Haas BJ et al. Transcriptional divergence of the duplicated oxidative stress?responsive genes in the Arabidopsis genome. The Plant Journal. 2005;41(2):212-20. https://doi.org/10.1111/j.1365-313X.2004.02295.x
  83. Pulido P, Zagari N, Manavski N, Gawronski P, Matthes A, Scharff LB et al. Chloroplast ribosome associated supports translation under stress and interacts with the ribosomal 30S subunit. Plant Physiology. 2018;177(4):1539-54. https://doi.org/10.1104/pp.18.00602
  84. Ding Y, Liu N, Virlouvet L, Riethoven J-J, Fromm M, Avramova Z. Four distinct types of dehydration stress memory genes in Arabidopsis thaliana. BMC Plant Biology. 2013;13(1):229. https://doi.org/10.1186/1471-2229-13-229
  85. Martínez-Ballesta M, Moreno-Fernández DA, Castejón D, Ochando C, Morandini PA, Carvajal M. The impact of the absence of aliphatic glucosinolates on water transport under salt stress in Arabidopsis thaliana. Frontiers in Plant Science. 2015;6:524. https://doi.org/10.3389/fpls.2015.00524
  86. Taochy C, Gaillard I, Ipotesi E, Oomen R, Leonhardt N, Zimmermann S et al. The Arabidopsis root stele transporter NPF2. 3 contributes to nitrate translocation to shoots under salt stress. The Plant Journal. 2015;83(3):466-79. https://doi.org/10.1111/tpj.12901
  87. Moreno JE, Moreno-Piovano G, Chan RL. The antagonistic basic helix-loop-helix partners BEE and IBH1 contribute to control plant tolerance to abiotic stress. Plant Science. 2018;271:143-50. https://doi.org/10.1016/j.plantsci.2018.03.024
  88. Chan CW, Wohlbach DJ, Rodesch MJ, Sussman MR. Transcriptional changes in response to growth of Arabidopsis in high external calcium. FEBS Letters. 2008;582(6):967-76. https://doi.org/10.1016/j.febslet.2008.02.043

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