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Comparative de novo transcriptome analysis identifies salinity stress responsive genes and metabolic pathways in sugarcane and its wild relative Erianthus arundinaceus [Retzius] Jeswiet

  • 1.

    Singh, A. et al. Phytochemical profile of sugarcane and its potential health aspects. Pharmacogn. Rev. 9, 45–54 (2015).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 2.

    Eggleston, G. Positive aspects of cane sugar and sugar cane derived products in food and nutrition. J. Agric. Food Chem. 66, 4007–4012 (2018).

    CAS 
    PubMed 

    Google Scholar 

  • 3.

    FAO. Area, production and productivity of livestock, Food and Agriculture Organization of United Nations. Food and Agriculture Organization of the United Nations, Database on Crops http://www.fao.org/faostat/en/#data/QC (2019).

  • 4.

    Zaman, M., Shahid, S. A. & Heng, L. Soil Salinity: Historical Perspectives and a World Overview of the Problem. in Guideline for Salinity Assessment, Mitigation and Adaptation Using Nuclear and Related Techniques (eds. Zaman, M., Shahid, S. A. & Heng, L.) 43.53 (Springer Nature Switzerland AG, 2018). doi:https://doi.org/10.1007/978-3-319-96190-3.

  • 5.

    Munns, R. & Tester, M. Mechanisms of salinity tolerance. Annu. Rev. Plant Biol. 59, 651–681 (2008).

    CAS 
    PubMed 

    Google Scholar 

  • 6.

    Wahid, A., Rao, A. U. R. & Rasul, E. Identification of salt tolerance traits in sugarcane lines. F. Crop. Res. 54, 9–17 (1997).

    Google Scholar 

  • 7.

    Lingle, S. E. & Wiegand, C. L. Soil salinity and sugarcane juice quality. F. Crop. Res. 54, 259–268 (1997).

    Google Scholar 

  • 8.

    Mahajan, S., Pandey, G. K. & Tuteja, N. Calcium- and salt-stress signaling in plants: Shedding light on SOS pathway. Arch. Biochem. Biophys. 471, 146–158 (2008).

    CAS 
    PubMed 

    Google Scholar 

  • 9.

    Manishankar, P., Wang, N., Köster, P., Alatar, A. A. & Kudla, J. Calcium signaling during salt stress and in the regulation of ion homeostasis. J. Exp. Bot. 69, 4215–4226 (2018).

    CAS 

    Google Scholar 

  • 10.

    Lamers, J., Meer, T. V. & Der & Testerink, C.,. How plants sense and respond to stressful environments. Plant Physiol. 182, 1624–1635 (2020).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 11.

    Liang, W., Ma, X., Wan, P. & Liu, L. Biochemical and biophysical research communications plant salt-tolerance mechanism: A review. Biochem. Biophys. Res. Commun. 495, 286–291 (2018).

    CAS 
    PubMed 

    Google Scholar 

  • 12.

    Gupta, B. & Huang, B. Mechanism of salinity tolerance in plants: Physiological, biochemical, and molecular characterization. Int. J. Genom. 2014, 2 (2014).

    Google Scholar 

  • 13.

    Unamba, C. I. N., Nag, A. & Sharma, R. K. Next generation sequencing technologies: The doorway to the unexplored genomics of non-model plants. Front. Plant Sci. 6(1074), 1–16 (2015).

    Google Scholar 

  • 14.

    Augustine, S. M., Cherian, A. V., Syamaladevi, D. P. & Subramonian, N. Erianthus arundinaceus HSP70 (EaHSP70) acts as a key regulator in the formation of anisotropic interdigitation in sugarcane (Saccharum spp. hybrid) in response to drought stress. Plant Cell Physiol. 56, 2368–2380 (2015).

    CAS 
    PubMed 

    Google Scholar 

  • 15.

    Manoj, V. M. et al. Comparative analysis of glyoxalase pathway genes in Erianthus arundinaceus and commercial sugarcane hybrid under salinity and drought conditions. BMC Genom. 19, 1–16 (2019).

    Google Scholar 

  • 16.

    Wang, W. et al. Sweetcane (Erianthus arundinaceus) as a native bioenergy crop with environmental remediation potential in southern China: A review. GCB Bioenergy 11, 1012–1025 (2019).

    Google Scholar 

  • 17.

    Ram, B., Sreenivasan, T. V., Sahi, B. K. & Singh, N. Introgression of low temperature tolerance and red rot resistance from Erianthus in sugarcane. Euphytica 122, 145–153 (2001).

    Google Scholar 

  • 18.

    Cai, Q. et al. Verification of the introgression of Erianthus arundinaceus germplasm into sugarcane using molecular markers. Plant Breed. 124, 322–328 (2005).

    CAS 

    Google Scholar 

  • 19.

    Augustine, S. M. et al. Erianthus arundinaceus HSP70 (EaHSP70) overexpression increases drought and salinity tolerance in sugarcane (Saccharum spp. hybrid). Plant Sci. 232, 23–34 (2015).

    CAS 
    PubMed 

    Google Scholar 

  • 20.

    Augustine, S. M. et al. Overexpression of EaDREB2 and pyramiding of EaDREB2 with the pea DNA helicase gene (PDH45) enhance drought and salinity tolerance in sugarcane (Saccharum spp. hybrid). Plant Cell Rep. 34, 247–263 (2015).

    CAS 
    PubMed 

    Google Scholar 

  • 21.

    Narayan, J. A. et al. Isolation and characterization of water-deficit stress-responsive α-expansin 1 (EXPA1) gene from Saccharum complex. 3 Biotech 9, 186 (2019).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 22.

    Anunathini, P. et al. In silico characterisation and functional validation of chilling tolerant divergence 1 (COLD1) gene in monocots during abiotic stress. Funct. Plant Biol. 46, 524–532 (2019).

    CAS 

    Google Scholar 

  • 23.

    Dharshini, S. et al. Root transcriptome analysis of Saccharum spontaneum uncovers key genes and pathways in response to low-temperature stress. Environ. Exp. Bot. 171, 103935 (2020).

    CAS 

    Google Scholar 

  • 24.

    Thirugnanasambandam, P. P., Hoang, N. V., Furtado, A., Botha, F. C. & Henry, R. J. Association of variation in the sugarcane transcriptome with sugar content. BMC Genom. 18, 1–22 (2017).

    Google Scholar 

  • 25.

    Cardoso-Silva, C. B. et al. De novo assembly and transcriptome analysis of contrasting sugarcane varieties. PLoS ONE 9, 1–10 (2014).

    Google Scholar 

  • 26.

    Santa Brigida, A. B. et al. Sugarcane transcriptome analysis in response to infection caused by Acidovorax avenae subsp. avenae. PLoS ONE 11, 1–30 (2016).

    Google Scholar 

  • 27.

    Que, Y., Su, Y., Guo, J., Wu, Q. & Xu, L. A global view of transcriptome dynamics during Sporisorium scitamineum challenge in sugarcane by RNA-seq. PLoS ONE 9, 1–18 (2014).

    Google Scholar 

  • 28.

    Kasirajan, L., Hoang, N. V., Furtado, A., Botha, F. C. & Henry, R. J. Transcriptome analysis highlights key differentially expressed genes involved in cellulose and lignin biosynthesis of sugarcane genotypes varying in fiber content. Sci. Rep. 8, 1–17 (2018).

    CAS 

    Google Scholar 

  • 29.

    Nair, N. V. & Somarajan, K. G. Diversity of Saccharum germplasm in Kerala, India. Plant Genet. Resour. Newsl. 135, 40–43 (2003).

    Google Scholar 

  • 30.

    Vasantha, S., Venkataramana, S., Gururaja Rao, P. N. & Gomathi, R. Long term salinity effect on growth, photosynthesis and osmotic characteristics in sugarcane. Sugar Tech. 12, 5–8 (2010).

    CAS 

    Google Scholar 

  • 31.

    Brindha, C., Srinivasavedantham, V., Arun, K. R. & Tayade, A. S. Characterization of the salt overly sensitive pathway genes in sugarcane under salinity stress. Physiol. Plant. 171, 677–687 (2021).

    CAS 
    PubMed 

    Google Scholar 

  • 32.

    Parida, A. K., Veerabathini, S. K., Kumari, A. & Agarwal, P. K. Physiological, anatomical and metabolic implications of salt tolerance in the halophyte Salvadora persica under hydroponic culture condition. Front. Plant Sci. 7, 1–18 (2016).

    Google Scholar 

  • 33.

    Silva, B. R. S., Batista, B. L. & Lobato, A. K. S. Anatomical changes in stem and root of soybean plants submitted to salt stress. Plant Biol. 23, 57–65 (2021).

    CAS 
    PubMed 

    Google Scholar 

  • 34.

    Simão, F. A., Waterhouse, R. M., Ioannidis, P., Kriventseva, E. V. & Zdobnov, E. M. BUSCO: Assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31, 3210–3212 (2015).

    PubMed 

    Google Scholar 

  • 35.

    Waterhouse, R. M., Seppey, M., Sim, F. A. & Ioannidis, P. BUSCO applications from quality assessments to gene prediction and phylogenomics letter fast track. Mol. Biol. Evol. 35, 543–548 (2017).

    PubMed Central 

    Google Scholar 

  • 36.

    Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B 57, 289–300 (1995).

    MathSciNet 
    MATH 

    Google Scholar 

  • 37.

    Götz, S. et al. High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res. 36, 3420–3435 (2008).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 38.

    Liu, Y., Wang, L., Zhang, T., Yang, X. & Li, D. Functional characterization of KS-type dehydrin ZmDHN13 and its related conserved domains under oxidative stress. Sci. Rep. 7, 1–10 (2017).

    ADS 

    Google Scholar 

  • 39.

    Arias, C. L. et al. NADP-dependent malic enzyme 1 participates in the abscisic acid response in arabidopsis thaliana. Front. Plant Sci. 871, 1–11 (2018).

    ADS 

    Google Scholar 

  • 40.

    Burlat, V., Kwon, M., Davin, L. B. & Lewis, N. G. Dirigent proteins and dirigent sites in lignifying tissues. Phytochemistry 57, 883–897 (2001).

    CAS 
    PubMed 

    Google Scholar 

  • 41.

    Luptovčiak, I., Komis, G., Takáč, T., Ovečka, M. & Šamaj, J. Katanin: A sword cutting microtubules for cellular, developmental, and physiological purposes. Front. Plant Sci. 8(1982), 1–10 (2017).

    Google Scholar 

  • 42.

    Saxena, P., Srivastava, R. P. & Sharma, M. L. Studies on salinity stress tolerance in sugarcane varieties. Sugar Tech 12, 59–63 (2010).

    CAS 

    Google Scholar 

  • 43.

    Chiconato, D. A. & da Silveira Sousa Junior, G., dos Santos, D. M. M. & Munns, R.,. Adaptation of sugarcane plants to saline soil. Environ. Exp. Bot. 162, 201–211 (2019).

    CAS 

    Google Scholar 

  • 44.

    Neves-Piestun, B. G. & Bernstein, N. Salinity-induced inhibition of leaf elongation in maize is not mediated by changes in cell wall acidification capacity. Plant Physiol. 125, 1419–1428 (2001).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 45.

    de Lacerda, C. F., Cambraia, J., Oliva, M. A., Ruiz, H. A. & Prisco, J. T. Solute accumulation and distribution during shoot and leaf development in two sorghum genotypes under salt stress. Environ. Exp. Bot. 49, 107–120 (2003).

    Google Scholar 

  • 46.

    Ashraf, M. & Foolad, M. R. Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ. Exp. Bot. 59, 206–216 (2007).

    CAS 

    Google Scholar 

  • 47.

    Barzegargolchini, B., Movafeghi, A., Dehestani, A. & Mehrabanjoubani, P. Increased cell wall thickness of endodermis and protoxylem in Aeluropus littoralis roots under salinity: The role of LAC4 and PER64 genes. J. Plant Physiol. 218, 127–134 (2017).

    CAS 
    PubMed 

    Google Scholar 

  • 48.

    Sharma, S. K. Soil salinity effects on transpiration and net photosynthetic rates, stomatal conductance and Na+ and Cl- contents in durum wheat. Biol. Plant. 38, 519 (1996).

    Google Scholar 

  • 49.

    Khan, S., Li, M., Wang, S. & Yin, H. Revisiting the role of plant transcription factors in the battle against abiotic stress. Int. J. Mol. Sci. J. Mol. Sci. 19(1634), 1–29 (2018).

    CAS 

    Google Scholar 

  • 50.

    Wen, W. et al. Switchgrass PvDREB1C plays opposite roles in plant cold and salt tolerance in transgenic tobacco. He 155, 1–12 (2018).

    Google Scholar 

  • 51.

    de Cabral, G. A. L. et al. First expressed TFome of physic nut (Jatropha curcas L.) after salt stimulus. Plant Mol. Biol. Rep. 38, 189–208 (2020).

    CAS 

    Google Scholar 

  • 52.

    Ramegowda, V. et al. GBF3 transcription factor imparts drought tolerance in Arabidopsis thaliana. Sci. Rep. 7(9148), 1–13 (2017).

    CAS 

    Google Scholar 

  • 53.

    He, T. et al. Gene-set association and epistatic analyses reveal complex gene interaction networks affecting flowering time in a worldwide barley collection. J. Exp. Bot. 70, 5603–5616 (2019).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 54.

    Chano, V., de Heredia, U. L., Collada, C. & Álvaro, S. Transcriptomic analysis of juvenile wood formation during the growing season in Pinus canariensis. Holzforschung 71, 919–937 (2017).

    CAS 

    Google Scholar 

  • 55.

    Badhan, S., Kole, P., Ball, A. & Mantri, N. Plant Physiology and Biochemistry RNA sequencing of leaf tissues from two contrasting chickpea genotypes reveals mechanisms for drought tolerance. Plant Physiol. Biochem. 129, 295–304 (2018).

    CAS 
    PubMed 

    Google Scholar 

  • 56.

    Zhou, F., Zhang, Y., Tang, W., Wang, M. & Gao, T. Transcriptomics analysis of the flowering regulatory genes involved in the herbicide resistance of Asia minor bluegrass (Polypogon fugax ). BMC Genom. 18(953), 1–13 (2017).

    Google Scholar 

  • 57.

    He, Y. et al. Jasmonic acid-mediated defense suppresses brassinosteroid-mediated susceptibility to Rice black streaked dwarf virus infection in rice. New Phytol. 214, 388–399 (2017).

    CAS 
    PubMed 

    Google Scholar 

  • 58.

    Xie, C. et al. KOBAS 2.0: A web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Res. https://doi.org/10.1093/nar/gkr483 (2011).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 59.

    Jonak, C. et al. Stress signaling in plants: A mitogen-activated protein kinase pathway is activated by cold and drought. Proc. Natl. Acad. Sci. U. S. A. 93, 11274–11279 (1996).

    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 60.

    Sinha, A. K., Jaggi, M., Raghuram, B. & Tuteja, N. Mitogen-activated protein kinase signaling in plants under abiotic stress. Plant Signal. Behav. 6, 196–203 (2011).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 61.

    Ali, A. et al. Genome-wide analysis of mitogen-activated protein ( MAP ) kinase gene family expression in response to biotic and abiotic stresses in sugarcane. Physiol. Plant. 171, 86–107 (2021).

    CAS 
    PubMed 

    Google Scholar 

  • 62.

    Manohar, M. et al. Members of the abscisic acid co-receptor PP2C protein family mediate salicylic acid—abscisic acid crosstalk. Plant Direct 1, 1–14 (2017).

    Google Scholar 

  • 63.

    Nakagami, H., Soukupová, H., Schikora, A., Žárský, V. & Hirt, H. A mitogen-activated protein kinase kinase kinase mediates reactive oxygen species homeostasis in Arabidopsis. J. Biol. Chem. 281, 38697–38704 (2006).

    CAS 
    PubMed 

    Google Scholar 

  • 64.

    Takahashi, Y. et al. MAP3 Kinase-dependent SnRK2-kinase activation is required for abscisic acid signal transduction and rapid osmotic stress response. Nat. Commun. 11(12), 1–12 (2020).

    Google Scholar 

  • 65.

    Binder, B. M., Rodríguez, F. I. & Bleecker, A. B. The copper transporter RAN1 is essential for biogenesis of ethylene receptors in Arabidopsis. J. Biol. Chem. 285, 37263–37270 (2010).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 66.

    Tao, J. J. et al. The role of ethylene in plants under salinity stress. Front. Plant Sci. 6, 1–12 (2015).

    Google Scholar 

  • 67.

    Lou, D., Wang, H. & Yu, D. The sucrose non-fermenting-1-related protein kinases SAPK1 and SAPK2 function collaboratively as positive regulators of salt stress tolerance in rice. BMC Plant Biol. 18(203), 1–17 (2018).

    ADS 

    Google Scholar 

  • 68.

    Akbudak, M. A., Yildiz, S. & Filiz, E. Genomics Pathogenesis related protein-1 ( PR-1) genes in tomato (Solanum lycopersicum L.): Bioinformatics analyses and expression profiles in response to drought stress. Genomics 112, 4089–4099 (2020).

    CAS 
    PubMed 

    Google Scholar 

  • 69.

    Isah, T. Stress and defense responses in plant secondary metabolites production. Biol. Res. 52, 1–25 (2019).

    CAS 

    Google Scholar 

  • 70.

    Sytar, O., Mbarki, S., Zivcak, M. & Brestic, M. The Involvement of Different Secondary Metabolites in Salinity Tolerance of Crops. in Salinity Responses and Tolerance in Plants, Volume 2 (eds. Kumar, V., Wani, S. H., Suprasanna, P. & Tran, L.-S. P.) vol. 2 21–49 (Springer International Publishing AG, 2018).

  • 71.

    Marondedze, C., Thomas, L., Gehring, C. & Lilley, K. S. Changes in the Arabidopsis RNA-binding proteome reveal novel stress response mechanisms. BMC Plant Biol. 19, 1–11 (2019).

    Google Scholar 

  • 72.

    Wu, X. et al. Gamma-aminobutyric acid ( GABA ) alleviates salt damage in tomato by modulating Na + uptake, the GAD gene, amino acid synthesis and reactive oxygen species metabolism. BMC Plant Biol. 20, 1–21 (2020).

    Google Scholar 

  • 73.

    Yang, Z. et al. Overexpression of β-ketoacyl-CoA synthase from Vitis vinifera L. Improves salt tolerance in Arabidopsis thaliana. Front. Plant Sci. 11, 1–11 (2020).

    CAS 

    Google Scholar 

  • 74.

    Almaghamsi, A., Nosarzewski, M., Kanayama, Y. & Archbold, D. D. Effects of abiotic stresses on sorbitol biosynthesis and metabolism in tomato (Solanum lycopersicum). Funct. Plant Biol. 48, 286–297 (2021).

    CAS 
    PubMed 

    Google Scholar 

  • 75.

    Stepansky, A. & Galili, G. Synthesis of the arabidopsis bifunctional lysine-ketoglutarate reductase/saccharopine dehydrogenase enzyme of lysine catabolism is concertedly regulated by metabolic and stress-associated signals. Plant Physiol. 133, 1407–1415 (2003).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 76.

    Pan, J. et al. Comparative proteomic investigation of drought responses in foxtail millet. BMC Plant Biol. 18(35), 1–19 (2018).

    CAS 

    Google Scholar 

  • 77.

    Hirooka, K., Bamba, T., Fukusaki, E. & Kobayashi, A. Cloning and kinetic characterization of Arabidopsis thaliana solanesyl diphosphate diphosphate synthase. Biochem. J. 686, 679–686 (2003).

    Google Scholar 

  • 78.

    Li, P. et al. The Arabidopsis UDP-glycosyltransferases UGT79B2 and UGT79B3, contribute to cold, salt and drought stress tolerance via modulating anthocyanin accumulation. Plant J. 89, 85–103 (2017).

    CAS 
    PubMed 

    Google Scholar 

  • 79.

    Tian, T. et al. AgriGO v2.0: A GO analysis toolkit for the agricultural community, 2017 update. Nucleic Acids Res. 45, W122–W129 (2017).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 80.

    Shi, P. & Gu, M. Transcriptome analysis and differential gene expression profiling of two contrasting quinoa genotypes in response to salt stress. BMC Plant Biol. 20(568), 1–15 (2020).

    CAS 

    Google Scholar 

  • 81.

    Liu, S. G., Zhu, D. Z., Chen, G. H., Gao, X. Q. & Zhang, X. S. Disrupted actin dynamics trigger an increment in the reactive oxygen species levels in the Arabidopsis root under salt stress. Plant Cell Rep. 31, 1219–1226 (2012).

    CAS 
    PubMed 

    Google Scholar 

  • 82.

    Frey, N. F. et al. Plasma membrane calcium ATPases are important components of receptor-mediated signaling in plant immune responses and development. Plant Physiol. 159, 798–809 (2012).

    Google Scholar 

  • 83.

    Endler, A. et al. A mechanism for sustained cellulose synthesis during salt stress. Cell 162, 1353–1364 (2015).

    CAS 
    PubMed 

    Google Scholar 

  • 84.

    Fan, Y. et al. Over-expression of a plasma membrane H+-ATPase SpAHA1 conferred salt tolerance to transgenic Arabidopsis. Protoplasma 255, 1827–1837 (2018).

    CAS 
    PubMed 

    Google Scholar 

  • 85.

    Verissimo, A. F. & Daldal, F. Cytochrome c biogenesis system I: An intricate process catalyzed by a maturase supercomplex?. Biochim. Biophys. Acta Bioenerg. 1837, 989–998 (2014).

    CAS 

    Google Scholar 

  • 86.

    Zhao, Z. & Assmann, S. M. The glycolytic enzyme, phosphoglycerate mutase, has critical roles in stomatal movement, vegetative growth, and pollen production in Arabidopsis thaliana. J. Exp. Bot. 62, 5179–5189 (2011).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 87.

    Grudkowska, M. & Zagdańska, B. Multifunctional role of plant cysteine proteinases. Acta Biochim. Pol. 51, 609–624 (2004).

    CAS 
    PubMed 

    Google Scholar 

  • 88.

    Yamada, H. et al. The arabidopsis AHK4 histidine kinase is a cytokinin-binding receptor that transduces cytokinin signals across the membrane. Plant Cell Physiol. 42, 1017–1023 (2001).

    CAS 
    PubMed 

    Google Scholar 

  • 89.

    Wang, X. et al. The roles of endomembrane trafficking in plant abiotic stress responses. J. Integr. Plant Biol. 62, 55–69 (2020).

    PubMed 

    Google Scholar 

  • 90.

    Niopek-Witz, S., Deppe, J., Lemieux, M. J. & Möhlmann, T. Biochemical characterization and structure-function relationship of two plant NCS2 proteins, the nucleobase transporters NAT3 and NAT12 from Arabidopsis thaliana. Biochim. Biophys. Acta Biomembr. 1838, 3025–3035 (2014).

    CAS 

    Google Scholar 

  • 91.

    Yang, H., Krebs, M., Stierhof, Y. D. & Ludewig, U. Characterization of the putative amino acid transporter genes AtCAT2, 3 & 4: The tonoplast localized AtCAT2 regulates soluble leaf amino acids. J. Plant Physiol. 171, 594–601 (2014).

    CAS 
    PubMed 

    Google Scholar 

  • 92.

    McMahon, H. T. & Boucrot, E. Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat. Rev. Mol. Cell Biol. 12, 517–533 (2011).

    CAS 

    Google Scholar 

  • 93.

    Shen, L. et al. CaCDPK15 positively regulates pepper responses to Ralstonia solanacearum inoculation and forms a positive-feedback loop with CaWRKY40 to amplify defense signaling. Sci. Rep. 6, 1–12 (2016).

    CAS 

    Google Scholar 

  • 94.

    Nguyen, H. T., Leipner, J., Stamp, P. & Guerra-Peraza, O. Low temperature stress in maize (Zea mays L.) induces genes involved in photosynthesis and signal transduction as studied by suppression subtractive hybridization. Plant Physiol. Biochem. 47, 116–122 (2009).

    PubMed 

    Google Scholar 

  • 95.

    Ahn, C. S., Han, A. J. A. & Pai, H. S. Characterization of in vivo functions of Nicotiana benthamiana RabE1. Planta 237, 161–172 (2013).

    CAS 
    PubMed 

    Google Scholar 

  • 96.

    Geisler, D. A. et al. Downregulation of the δ-subunit reduces mitochondrial ATP synthase levels, alters respiration, and restricts growth and gametophyte development in Arabidopsis. Plant Cell 24, 2792–2811 (2012).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 97.

    Xu, N. et al. The arabidopsis NRG2 protein mediates nitrate signaling and interacts with and regulates key nitrate regulators. 28, 485–504 (2016).

  • 98.

    Wang, W. et al. The Arabidopsis exocyst subunits EXO70B1 and EXO70B2 regulate FLS2 homeostasis at the plasma membrane. New Phytol. 227, 529–544 (2020).

    CAS 
    PubMed 

    Google Scholar 

  • 99.

    Ilk, N., Ding, J., Ihnatowicz, A., Koornneef, M. & Reymond, M. Natural variation for anthocyanin accumulation under high-light and low-temperature stress is attributable to the ENHANCER OF AG-4 2 (HUA2) locus in combination with production of anthocyanin pigment1 (PAP1) and PAP2. New Phytol. 206, 422–435 (2015).

    CAS 
    PubMed 

    Google Scholar 

  • 100.

    Shavrukov, Y. Salt stress or oceanica salt shock: Which genes are we studying ? In Posidonia cadmium induces changes in DNA methylation and chromatin patterning. J. Exp. Bot. 64, 119–127 (2013).

    CAS 
    PubMed 

    Google Scholar 

  • 101.

    Soltys-Kalina, D., Plich, J., Strzelczyk-Żyta, D., Śliwka, J. & Marczewski, W. The effect of drought stress on the leaf relative water content and tuber yield of a half-sib family of ‘Katahdin’-derived potato cultivars. Breed. Sci. 66, 328–331 (2016).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 102.

    Bates, L. S., Waldren, R. P. & Teare, I. D. Rapid determination of free proline for water-stress studies. Plant Soil 39, 205–207 (1973).

    CAS 

    Google Scholar 

  • 103.

    Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: A flexible trimmer for illumina sequence data. Bioinformatics 30, 2114–2120 (2014).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 104.

    Pereira-Santana, A. et al. Transcriptional profiling of sugarcane leaves and roots under progressive osmotic stress reveals a regulated coordination of gene expression in a spatiotemporal manner. PLoS ONE 12, 1–25 (2017).

    Google Scholar 

  • 105.

    Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 106.

    Grabherr, M. G. et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 29, 644–652 (2011).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 107.

    Gurevich, A., Saveliev, V., Vyahhi, N. & Tesler, G. QUAST: Quality assessment tool for genome assemblies. Bioinformatics 29, 1072–1075 (2013).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 108.

    Li, W. & Godzik, A. Cd-hit: A fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22, 1658–1659 (2006).

    CAS 
    PubMed 

    Google Scholar 

  • 109.

    Geniza, M. & Jaiswal, P. Tools for building de novo transcriptome assembly. Curr. Plant Biol. 11–12, 41–45 (2017).

    Google Scholar 

  • 110.

    Hoang, N. V., Furtado, A., Thirugnanasambandam, P. P., Botha, F. C. & De Henry, R. J. novo assembly and characterizing of the culm-derived meta-transcriptome from the polyploid sugarcane genome based on coding transcripts. Heliyon 4, 1–36 (2018).

    Google Scholar 

  • 111.

    Li, B. & Dewey, C. N. RSEM: Accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform. 12(323), 1–16 (2011).

    Google Scholar 

  • 112.

    Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15(550), 1–21 (2014).

    Google Scholar 

  • 113.

    Love, M. I., Anders, S. & Huber, W. Analyzing RNA-seq data with DESeq2. https://bioconductor.org/packages/release/bioc/vignettes/DESeq2/inst/doc/DESeq2.html#why-un-normalized-counts (2021).

  • 114.

    Kanehisa, M. & Goto, S. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 28, 27–30 (2000).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 115.

    Kanehisa, M. Toward understanding the origin and evolution of cellular organisms. Protein Sci. 28, 1947–1951 (2019).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 116.

    Kanehisa, M., Furumichi, M., Sato, Y., Ishiguro-Watanabe, M. & Tanabe, M. KEGG: Integrating viruses and cellular organisms. Nucleic Acids Res. 49, D545–D551 (2021).

    CAS 
    PubMed 

    Google Scholar 

  • 117.

    Owczarzy, R. et al. IDT SciTools: A suite for analysis and design of nucleic acid oligomers. Nucleic Acids Res. 36, 163–169 (2008).

    Google Scholar 

  • 118.

    Schultz, J., Milpetz, F., Bork, P. & Ponting, C. P. SMART, a simple modular architecture research tool: Identification of signaling domains. Proc. Natl. Acad. Sci. U. S. A. 95, 5857–5864 (1998).

    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 119.

    Selvarajan, D. et al. Differential gene expression profiling through transcriptome approach of Saccharum spontaneum L. under low temperature stress reveals genes potentially involved in cold acclimation. 3 Biotech 8, 1–18 (2018).

    Google Scholar 

  • 120.

    Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25, 402–408 (2001).

    CAS 

    Google Scholar 

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