Identification of key genes involved in the establishment and maintenance of heat stress memory in Arabidopsis seedlings using microarray data

Arif, M., Li, Z., Luo, Q., Li, L., Shen, Y., & Men, S. (2021). The BAG2 and BAG6 genes are involved in multiple abiotic stress tolerances in Arabidopsis thaliana. International Journal of Molecular Sciences, 22(11), 5856. Bäurle, I. (2016). Plant heat adaptation: priming in response to heat stress. F1000Research, 5. Bäurle, I. (2018, November). Can’t remember to forget you: chromatin-based priming of somatic stress responses. In Seminars in cell & developmental biology (Vol. 83, pp. 133-139). Academic Press. Bäurle, I. and Trindade, I. (2020). Chromatin regulation of somatic abiotic stress memory. Journal of Experimental Botany, 71(17): 5269-5279. Brzezinka, K., Altmann, S. and Bäurle, I. (2019). BRUSHY1/TONSOKU/MGOUN3 is required for heat stress memory. Plant, Cell & Environment, 42(3): 771-781. Carrigan, P.E., Sikkink, L.A., Smith, D.F. and Ramirez‐Alvarado, M. (2006). Domain: domain interactions within Hop, the Hsp70/Hsp90 organizing protein, are required for protein stability and structure. Protein Science, 15(3): 522-532. Charng, Y.Y., Liu, H.C., Liu, N.Y., Hsu, F.C. and Ko, S.S. (2006). Arabidopsis Hsa32, a novel heat shock protein, is essential for acquired thermotolerance during long recovery after acclimation. Plant Physiology, 140(4):1297-1305. dos Santos, T.B. and Vieira, L.G.E. (2020). Involvement of the galactinol synthase gene in abiotic and biotic stress responses: A review on current knowledge. Plant Gene, 24: 100258. Dragovic, Z., Shomura, Y., Tzvetkov, N., Hartl, F.U. and Bracher, A. (2006). Fes1p acts as a nucleotide exchange factor for the ribosome-associated molecular chaperone Ssb1p. Biological Chemistry, 387(12): 1593-1600. Gowda, N.K.C., Kaimal, J.M., Masser, A.E. Kang, W., Friedländer, M.R. and Andréasson, C. (2016). Cytosolic splice isoform of Hsp70 nucleotide exchange factor Fes1 is required for the degradation of misfolded proteins in yeast. Molecular Biology of the Cell, 27(8): 1210-1219. Hall, D. (2020). On the nature of the optimal form of the holdase‐type chaperone stress response. FEBS Letters, 594(1): 43-66. Haslbeck, M., Weinkauf, S. and Buchner J. (2019). Small heat shock proteins: simplicity meets complexity. Journal of Biological Chemistry, 294(6): 2121-2132. Heidari, P., Ahmadizadeh, M. and NajafiZarrini, H. (2015). In Silico Analysis of Cis-regulatory Elements on co-expressed genes. Journal of Biological &. Environmental Sciences, 9(25): 1-9. Hilker, M., Schwachtje, J., Baier, M., Balazadeh, S., Bäurle, I., Geiselhardt, S., Hincha, D.K., Kunze, R., Mueller‐Roeber, B., Rillig, M.C. and Rolff, J. (2016). Priming and memory of stress responses in organisms lacking a nervous system. Biological Reviews, 91(4): 1118-1133. Jakoby, M., Weisshaar, B., Dröge-Laser, W., Vicente-Carbajosa, J., Tiedemann, J., Kroj, T. and Parcy, F. (2002). bZIP transcription factors in Arabidopsis. Trends in Plant Science, 7: 106–111 Khan, A., Khan, V., Pandey, K., Sopory, S.K. and Sanan-Mishra, N. (2022). Thermo-priming mediated cellular networks for abiotic stress management in plants. Frontiers in Plant Science, 13: 866409. Kushawaha, A.K, Khan, A., Sopory, S.K. and Sanan-Mishra, N. (2021). Priming by high temperature stress induces microRNA regulated heat shock modules indicating their involvement in thermopriming response in rice. Life (Basel), 11(4): 291. Lämke, J., Brzezinka, K., Altmann, S. and Bäurle, I. (2016a). A hit‐and‐run heat shock factor governs sustained histone methylation and transcriptional stress memory. EMBO Journal, 35(2): 162-175. Lämke, J., Brzezinka, K and Bäurle I. (2016b). HSFA2 orchestrates transcriptional dynamics after heat stress in Arabidopsis thaliana. Transcription, 7(4): 111–114 Lämke, J. and Bäurle, I. (2017). Epigenetic and chromatin-based mechanisms in environmental stress adaptation and stress memory in plants. Genome Biology, 18(1): 1-11. Lee, J. G. and Ye, Y. (2013). Bag6/Bat3/Scythe: A novel chaperone activity with diverse regulatory functions in protein biogenesis and degradation. Bioessays, 35: 377-385. Lin, M.Y., Chai, K.H., Ko, S.S., Kuang, L.Y., Lur, H.S. and Charng, Y.Y. (2014). A positive feedback loop between heat shock protein101 and heat stress-associated 32-kd protein modulates long-term acquired thermotolerance illustrating diverse heat stress responses in rice varieties. Plant Physiology, 164(4): 2045-2053. Ling, Y., Serrano, N., Gao, G., Atia, M., Mokhtar, M., Woo, Y.H., Bazin, J., Veluchamy, A., Benhamed, M. and Crespi, M. (2018). Thermopriming triggers splicing memory in Arabidopsis. Journal of Experimental Botany, 69(10): 2659-2675. Liu, Y., Zhang, A., Yin, H., Meng, Q., Yu, X., Huang, S., Wang, J., Ahmad, R., Liu, B. and Xu, Z.Y. (2018a). Trithorax‐group proteins ARABIDOPSIS TRITHORAX4 (ATX4) and ATX 5 function in abscisic acid and dehydration stress responses. New Phytologist, 217(4):1582-1597. Liu, H.C., Lämke, J., Lin, S.Y., Hung, M.J., Liu, K.M., Charng, Y.Y. and Bäurle, I. (2018b). Distinct heat shock factors and chromatin modifications mediate the organ‐autonomous transcriptional memory of heat stress. Plant Journal, 95(3): 401-413. Mayer, M. P. and Gierasch, L. M. (2019). Recent advances in the structural and mechanistic aspects of Hsp70 molecular chaperones. Journal of Biological Chemistry, 294: 2085–2097. Meiri, D., Breiman, A. (2009). Arabidopsis ROF1 (FKBP62) modulates thermotolerance by interacting with HSP90. 1 and affecting the accumulation of HsfA2‐regulated sHSPs. Plant Journal, 59(3): 387-399. Mishra, R.C. and Grover, A. (2016). ClpB/Hsp100 proteins and heat stress tolerance in plants. Critical Reviews in Biotechnology, 36(5): 862-874. Mogk, A., Bukau, B. and Kampinga, H.H. (2018). Cellular handling of protein aggregates by disaggregation machines. Molecular Cell, 69(2): 214-226. Nollen, E.A. and Morimoto, R.I. (2002). Chaperoning signaling pathways: molecular chaperones as stress-sensing 'heat shock' proteins. Journal of Cell Science, 115(14): 2809-2816. Oberkofler, V., Pratx, L. and Bäurle, I. (2021). Epigenetic regulation of abiotic stress memory: maintaining the good things while they last. Current Opinion in Plant Biology, 61: 102007. Panikulangara, T.J., Eggers-Schumacher, G., Wunderlich, M., Stransky, H. and Schöffl, F. (2004). Galactinol synthase 1. A novel heat shock factor target gene responsible for heat-induced synthesis of raffinose family oligosaccharides in Arabidopsis. Plant Physiology, 136(2):3148-3158. Parcerisa, I.L., Rosano, G.L. and Ceccarelli, E.A. (2020). Biochemical characterization of ClpB3, a chloroplastic disaggregase from Arabidopsis thaliana. Plant Molecular Biology, 104(4): 451-465. Ritchie, ME., Phipson, B., Wu, D.I., Hu, Y., Law, C.W., Shi, W. and Smyth, G.K. (2015). limma powers diferential expression analyses for RNA sequencing and microarray studies. Nucleic Acids Research, 43(7):e47 Rolly, N.K., Imran, Q.M., Shahid, M., Imran, M., Khan, M., Lee, S.U., Hussain, A., Lee, I.J. and Yun, B.W. (2020). Drought-induced AtbZIP62 transcription factor regulates drought stress response in Arabidopsis. Plant Physiology and Biochemistry, 156; 384–395. Sauer, R.T. and Baker, T.A. (2011). AAA+ proteases: ATP-fueled machines of protein destruction. Annual Review of Biochemistry, 80: 587-612. Sedaghatmehr, M. Mueller-Roeber, B. and Balazadeh, S. (2016). The plastid metalloprotease FtsH6 and small heat shock protein HSP21 jointly regulate thermomemory in Arabidopsis. Nature Communications, 7: 12439. Sequeira-Mendes, J., Aragüez, I., Peiró, R. Mendez-Giraldez, R., Zhang, X., Jacobsen, S.E., Bastolla, U. and Gutierrez, C. (2014). The functional topography of the Arabidopsis genome is organized in a reduced number of linear motifs of chromatin states. Plant Cell, 26(6): 2351-2366. Standaert, R. F., Galat, A., Verdine, G. L. and Schreiber, S. L. (1990). Molecular cloning and overexpression of the human FK506-binding protein FKBP. Nature, 346(6285): 671-674 Stief, A., Altmann, S., Hoffmann, K. et al. (2014a). Arabidopsis miR156 regulates tolerance to recurring environmental stress through SPL transcription factors. Plant Cell, 26(4) :1792-1807. Stief, A., Brzezinka, K., Lämke, J. and Bäurle, I. (2014b). Epigenetic responses to heat stress at different time scales and the involvement of small RNAs. Plant signaling & behavior, 9(10): e970430. Wang, W., Vinocur, B., Shoseyov, O. and Altman, A. (2004). Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends in Plant Science, 9(5): 244-252. Wu, T.Y., Juan, Y.T., Hsu, Y.H., Wu, S.H., Liao, H.T., Fung, R.W. and Charng, Y.Y. (2013). Interplay between heat shock proteins HSP101 and HSA32 prolongs heat acclimation memory posttranscriptionally in Arabidopsis.Plant Physiology,161(4):2075–2084. Yamaguchi, N. (2021). Heat memory in plants: histone modifications, nucleosome positioning and miRNA accumulation alter heat memory gene expression. Genes & Genetic Systems, 96(5): 229-235. Yamaguchi, N., Matsubara, S., Yoshimizu ,K., Seki, M., Hamada, K., Kamitani, M., Kurita, Y., Nomura, Y., Nagashima, K., Inagaki, S., Suzuki, T., Gan, E.S., To, T., Kakutani, T., Nagano, A.J., Satake, A. and Ito, T. (2021). H3K27me3 demethylases alter HSP22 and HSP17. 6C expression in response to recurring heat in Arabidopsis. Nature Communications, 12(1): 1-16. Yeh, C.H., Kaplinsky, N.J., Hu, C., Charng, Y.Y. (2012). Some like it hot, some like it warm: phenotyping to explore thermotolerance diversity. Plant Science, 195: 10-23. Zhang, X., Bernatavichute, Y.V., Cokus, S, Pellegrini, M., and Jacobsen, S.E. (2009). Genome-wide analysis of mono-, di- and trimethylation of histone H3 lysine 4 in Arabidopsis thaliana. Genome Biology, 10: 1-14. Zhang, J.X., Wang, C., Yang, C.Y. Wang, J.Y., Chen, L., Bao, X.M., Zhao, Y.X., Zhang, H. and Liu, J. (2010). The role of Arabidopsis AtFes1A in cytosolic Hsp70 stability and abiotic stress tolerance. Plant Journal, 62(4): 539-548. Zhang, B., Feng, C., Chen, L., Li, B., Zhang, X. and Yang X. (2022). Identification and functional analysis of bZIP genes in cotton response to drought stress. International Journal of Molecular Sciences, 28: 23(23):14894. Zhou, Y., Wang, Y., Xu, F. and Song, C. (2022). Small HSPs play an important role in crosstalk between HSF-HSP and ROS pathways in heat stress response through transcriptomic analysis in lilies (Lilium longiflorum). BMC Plant Biology, 22(1): 202. Zhuang, Y., Wei, M., Ling, C., Liu, Y., Amin, A. K., Li, P., ... & Wang, S. (2021). EGY3 mediates chloroplastic ROS homeostasis and promotes retrograde signaling in response to salt stress in Arabidopsis. Cell Reports, 36(2), 109384. Zuiderweg, E. R., Hightower, L. E., & Gestwicki, J. E. (2017). The remarkable multivalency of the Hsp70 chaperones. Cell Stress and Chaperones, 22, 173-189.