دورية أكاديمية
Histone variant HTB4 delays leaf senescence by epigenetic control of Ib bHLH transcription factor-mediated iron homeostasis.
العنوان: | Histone variant HTB4 delays leaf senescence by epigenetic control of Ib bHLH transcription factor-mediated iron homeostasis. |
---|---|
المؤلفون: | Yang Q; State Key Laboratory of Tree Genetics and Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, 100083, China., Wang T; State Key Laboratory of Tree Genetics and Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, 100083, China., Cao J; State Key Laboratory of Tree Genetics and Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, 100083, China., Wang HL; State Key Laboratory of Tree Genetics and Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, 100083, China., Tan S; State Key Laboratory of Tree Genetics and Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, 100083, China., Zhang Y; State Key Laboratory of Tree Genetics and Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, 100083, China., Park S; Department of New Biology, Daegu Gyeongbuk Institute of Science and Technology (DGIST), Daegu, 42988, South Korea., Park H; Department of New Biology, Daegu Gyeongbuk Institute of Science and Technology (DGIST), Daegu, 42988, South Korea., Woo HR; Department of New Biology, Daegu Gyeongbuk Institute of Science and Technology (DGIST), Daegu, 42988, South Korea.; New Biology Research Center, Daegu Gyeongbuk Institute of Science and Technology (DGIST), Daegu, 42988, South Korea., Li X; State Key Laboratory of Tree Genetics and Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, 100083, China., Xia X; State Key Laboratory of Tree Genetics and Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, 100083, China., Guo H; Department of Biology, Key Laboratory of Molecular Design for Plant Cell Factory of Guangdong Higher Education Institutes, Southern University of Science and Technology (SUSTech), Shenzhen, Guangdong, 518055, China., Li Z; State Key Laboratory of Tree Genetics and Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, 100083, China. |
المصدر: | The New phytologist [New Phytol] 2023 Oct; Vol. 240 (2), pp. 694-709. Date of Electronic Publication: 2023 Jun 02. |
نوع المنشور: | Journal Article; Research Support, Non-U.S. Gov't |
اللغة: | English |
بيانات الدورية: | Publisher: Wiley on behalf of New Phytologist Trust Country of Publication: England NLM ID: 9882884 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1469-8137 (Electronic) Linking ISSN: 0028646X NLM ISO Abbreviation: New Phytol Subsets: MEDLINE |
أسماء مطبوعة: | Publication: Oxford : Wiley on behalf of New Phytologist Trust Original Publication: London, New York [etc.] Academic Press. |
مواضيع طبية MeSH: | Arabidopsis*/metabolism , Arabidopsis Proteins*/genetics , Arabidopsis Proteins*/metabolism, Basic Helix-Loop-Helix Transcription Factors/genetics ; Basic Helix-Loop-Helix Transcription Factors/metabolism ; Histones/metabolism ; Plant Senescence ; Homeostasis ; Membrane Transport Proteins/metabolism ; Epigenesis, Genetic ; Gene Expression Regulation, Plant |
مستخلص: | Leaf senescence is an orderly process regulated by multiple internal factors and diverse environmental stresses including nutrient deficiency. Histone variants are involved in regulating plant growth and development. However, their functions and underlying regulatory mechanisms in leaf senescence remain largely unclear. Here, we found that H2B histone variant HTB4 functions as a negative regulator of leaf senescence. Loss of function of HTB4 led to early leaf senescence phenotypes that were rescued by functional complementation. RNA-seq analysis revealed that several Ib subgroup basic helix-loop-helix (bHLH) transcription factors (TFs) involved in iron (Fe) homeostasis, including bHLH038, bHLH039, bHLH100, and bHLH101, were suppressed in the htb4 mutant, thereby compromising the expressions of FERRIC REDUCTION OXIDASE 2 (FRO2) and IRON-REGULATED TRANSPORTER (IRT1), two important components of the Fe uptake machinery. Chromatin immunoprecipitation-quantitative polymerase chain reaction analysis revealed that HTB4 could bind to the promoter regions of Ib bHLH TFs and enhance their expression by promoting the enrichment of the active mark H3K4me3 near their transcriptional start sites. Moreover, overexpression of Ib bHLH TFs or IRT1 suppressed the premature senescence phenotype of the htb4 mutant. Our work established a signaling pathway, HTB4-bHLH TFs-FRO2/IRT1-Fe homeostasis, which regulates the onset and progression of leaf senescence. (© 2023 The Authors New Phytologist © 2023 New Phytologist Foundation.) |
التعليقات: | Comment in: New Phytol. 2023 Oct;240(2):461-463. (PMID: 37583252) |
References: | Balazadeh S, Riano-Pachon DM, Mueller-Roeber B. 2008. Transcription factors regulating leaf senescence in Arabidopsis thaliana. Plant Biology 10: 63-75. Berriri S, Gangappa SN, Kumar SV. 2016. SWR1 chromatin-remodeling complex subunits and H2A.Z have non-overlapping functions in immunity and gene regulation in Arabidopsis. Molecular Plant 9: 1051-1065. Cao J, Zhang Y, Tan S, Yang Q, Wang H-L, Xia X, Luo J, Guo H, Zhang Z, Li Z. 2022. LSD 4.0: an improved database for comparative studies of leaf senescence. Molecular Horticulture 2: 24. Clough SJ, Bent AF. 1998. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant Journal 16: 735-743. Connolly EL, Campbell NH, Grotz N, Prichard CL, Guerinot ML. 2003. Overexpression of the FRO2 ferric chelate reductase confers tolerance to growth on low iron and uncovers posttranscriptional control. Plant Physiology 133: 1102-1110. Connorton JM, Balk J, Rodriguez-Celma J. 2017. Iron homeostasis in plants - a brief overview. Metallomics 9: 813-823. Cui Y, Chen CL, Cui M, Zhou WJ, Wu HL, Ling HQ. 2018. Four IVa bHLH transcription factors are novel interactors of FIT and mediate JA inhibition of iron uptake in Arabidopsis. Molecular Plant 11: 1166-1183. Cutler SR, Ehrhardt DW, Griffitts JS, Somerville CR. 2000. Random GFP::cDNA fusions enable visualization of subcellular structures in cells of Arabidopsis at a high frequency. Proceedings of the National Academy of Sciences, USA 97: 3718-3723. Deal RB, Henikoff S. 2011. Histone variants and modifications in plant gene regulation. Current Opinion in Plant Biology 14: 116-122. Fan H, Zhang Z, Wang N, Cui Y, Sun H, Liu Y, Wu H, Zheng S, Bao S, Ling HQ. 2014. SKB1/PRMT5-mediated histone H4R3 dimethylation of Ib subgroup bHLH genes negatively regulates iron homeostasis in Arabidopsis thaliana. The Plant Journal 77: 209-221. Feng Z, Zhang B, Ding W, Liu X, Yang DL, Wei P, Cao F, Zhu S, Zhang F, Mao Y et al. 2013. Efficient genome editing in plants using a CRISPR/Cas system. Cell Research 23: 1229-1232. Feser J, Truong D, Das C, Carson JJ, Kieft J, Harkness T, Tyler JK. 2010. Elevated histone expression promotes life span extension. Molecular Cell 39: 724-735. Frith MC, Valen E, Krogh A, Hayashizaki Y, Carninci P, Sandelin A. 2008. A code for transcription initiation in mammalian genomes. Genome Research 18: 1-12. Gan S, Amasino RM. 1997. Making sense of senescence (molecular genetic regulation and manipulation of leaf senescence). Plant Physiology 113: 313-319. Gao F, Dubos C. 2021. Transcriptional integration of plant responses to iron availability. Journal of Experimental Botany 72: 2056-2070. Gao F, Robe K, Bettembourg M, Navarro N, Rofidal V, Santoni V, Gaymard F, Vignols F, Roschzttardtz H, Izquierdo E et al. 2020a. The transcription factor bHLH121 Interacts with bHLH105 (ILR3) and its closest homologs to regulate iron homeostasis in Arabidopsis. Plant Cell 32: 508-524. Gao F, Robe K, Dubos C. 2020b. Further insights into the role of bHLH121 in the regulation of iron homeostasis in Arabidopsis thaliana. Plant Signaling & Behavior 15: 1795582. Gao F, Robe K, Gaymard F, Izquierdo E, Dubos C. 2019. The transcriptional control of iron homeostasis in plants: a tale of bHLH transcription factors? Frontiers in Plant Science 10: 6. Gepstein S. 2004. Leaf senescence-not just a 'wear and tear' phenomenon. Genome Biology 5: 212. Gomez-Zambrano A, Merini W, Calonje M. 2019. The repressive role of Arabidopsis H2A.Z in transcriptional regulation depends on AtBMI1 activity. Nature Communications 10: 2828. Guo Y, Gan S. 2005. Leaf senescence: signals, execution, and regulation. Current Topics in Developmental Biology 71: 83-112. Guo Y, Gan SS. 2014. Translational researches on leaf senescence for enhancing plant productivity and quality. Journal of Experimental Botany 65: 3901-3913. Henikoff S, Smith MM. 2015. Histone variants and epigenetics. Cold Spring Harbor Perspectives in Biology 7: a019364. Higuchi K, Iwase J, Tsukiori Y, Nakura D, Kobayashi N, Ohashi H, Saito A, Miwa E. 2014. Early senescence of the oldest leaves of Fe-deficient barley plants may contribute to phytosiderophore release from the roots. Physiologia Plantarum 151: 313-322. Huang P, Li Z, Guo H. 2022. New advances in the regulation of leaf senescence by classical and peptide hormones. Frontiers in Plant Science 13: 923136. Jefferson RA, Kavanagh TA, Bevan MW. 1987. GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO Journal 6: 3901-3907. Jiang D, Borg M, Lorkovic ZJ, Montgomery SA, Osakabe A, Yelagandula R, Axelsson E, Berger F. 2020. The evolution and functional divergence of the histone H2B family in plants. PLoS Genetics 16: e1008964. Keskitalo J, Bergquist G, Gardestrom P, Jansson S. 2005. A cellular timetable of autumn senescence. Plant Physiology 139: 1635-1648. Khadka J, Pesok A, Grafi G. 2020. Plant histone HTB (H2B) variants in regulating chromatin structure and function. Plants 9: 1435. Kim HJ, Nam HG, Lim PO. 2016. Regulatory network of NAC transcription factors in leaf senescence. Current Opinion in Plant Biology 33: 48-56. Kim HJ, Park JH, Kim J, Kim JJ, Hong S, Kim J, Kim JH, Woo HR, Hyeon C, Lim PO et al. 2018. Time-evolving genetic networks reveal a NAC troika that negatively regulates leaf senescence in Arabidopsis. Proceedings of the National Academy of Sciences, USA 115: E4930-E4939. Kim J, Woo HR, Nam HG. 2016. Toward systems understanding of leaf senescence: an integrated multi-omics perspective on leaf senescence research. Molecular Plant 9: 813-825. Kim SA, LaCroix IS, Gerber SA, Guerinot ML. 2019. The iron deficiency response in Arabidopsis thaliana requires the phosphorylated transcription factor URI. Proceedings of the National Academy of Sciences, USA 116: 24933-24942. Kumar SV, Wigge PA. 2010. H2A.Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell 140: 136-147. Lei R, Li Y, Cai Y, Li C, Pu M, Lu C, Yang Y, Liang G. 2020. bHLH121 Functions as a direct link that facilitates the activation of FIT by bHLH IVc transcription factors for maintaining Fe homeostasis in Arabidopsis. Molecular Plant 13: 634-649. Li X, Zhang H, Ai Q, Liang G, Yu D. 2016. Two bHLH transcription factors, bHLH34 and bHLH104, regulate iron homeostasis in Arabidopsis thaliana. Plant Physiology 170: 2478-2493. Li Z, Peng J, Wen X, Guo H. 2013. Ethylene-insensitive3 is a senescence-associated gene that accelerates age-dependent leaf senescence by directly repressing miR164 transcription in Arabidopsis. Plant Cell 25: 3311-3328. Li Z, Zhang Y, Zou D, Zhao Y, Wang HL, Zhang Y, Xia X, Luo J, Guo H, Zhang Z. 2020. LSD 3.0: a comprehensive resource for the leaf senescence research community. Nucleic Acids Research 48: D1069-D1075. Li Z, Zhao Y, Liu X, Peng J, Guo H, Luo J. 2014. LSD 2.0: an update of the leaf senescence database. Nucleic Acids Research 42: D1200-D1205. Liang G, Zhang H, Li X, Ai Q, Yu D. 2017. bHLH transcription factor bHLH115 regulates iron homeostasis in Arabidopsis thaliana. Journal of Experimental Botany 68: 1743-1755. Lim PO, Kim HJ, Nam HG. 2007. Leaf senescence. Annual Review of Plant Biology 58: 115-136. Lingam S, Mohrbacher J, Brumbarova T, Potuschak T, Fink-Straube C, Blondet E, Genschik P, Bauer P. 2011. Interaction between the bHLH transcription factor FIT and ETHYLENE INSENSITIVE3/ETHYLENE INSENSITIVE3-LIKE1 reveals molecular linkage between the regulation of iron acquisition and ethylene signaling in Arabidopsis. Plant Cell 23: 1815-1829. Liu P, Zhang S, Zhou B, Luo X, Zhou XF, Cai B, Jin YH, Niu LJ, Cao X et al. 2019. The histone H3K4 demethylase JMJ16 represses leaf senescence in Arabidopsis. Plant Cell 31: 430-443. Liu W, Karemera NJU, Wu T, Yang Y, Zhang X, Xu X, Wang Y, Han Z. 2017a. The ethylene response factor AtERF4 negatively regulates the iron deficiency response in Arabidopsis thaliana. PLoS ONE 12: e0186580. Liu W, Li Q, Wang Y, Wu T, Yang Y, Zhang X, Han Z, Xu X. 2017b. Ethylene response factor AtERF72 negatively regulates Arabidopsis thaliana response to iron deficiency. Biochemical and Biophysical Research Communications 491: 862-868. Long TA, Tsukagoshi H, Busch W, Lahner B, Salt DE, Benfey PN. 2010. The bHLH transcription factor POPEYE regulates response to iron deficiency in Arabidopsis roots. Plant Cell 22: 2219-2236. Martire S, Banaszynski LA. 2020. The roles of histone variants in fine-tuning chromatin organization and function. Nature Reviews. Molecular Cell Biology 21: 522-541. Noh YS, Amasino RM. 1999. Identification of a promoter region responsible for the senescence-specific expression of SAG12. Plant Molecular Biology 41: 181-194. Park BS, Yao T, Seo JS, Wong ECC, Mitsuda N, Huang CH, Chua NH. 2018. Arabidopsis NITROGEN LIMITATION ADAPTATION regulates ORE1 homeostasis during senescence induced by nitrogen deficiency. Nature Plants 4: 898-903. Park EY, Tsuyuki KM, Parsons EM, Jeong J. 2020. PRC2-mediated H3K27me3 modulates shoot iron homeostasis in Arabidopsis thaliana. Plant Signaling & Behavior 15: 1784549. Robinson NJ, Procter CM, Connolly EL, Guerinot ML. 1999. A ferric-chelate reductase for iron uptake from soils. Nature 397: 694-697. Rodriguez-Celma J, Pan IC, Li W, Lan P, Buckhout TJ, Schmidt W. 2013. The transcriptional response of Arabidopsis leaves to Fe deficiency. Frontiers in Plant Science 4: 276. Rogakou EP, Sekeri-Pataryas KE. 1999. Histone variants of H2A and H3 families are regulated during in vitro aging in the same manner as during differentiation. Experimental Gerontology 34: 741-754. Saleh A, Alvarez-Venegas R, Avramova Z. 2008. An efficient chromatin immunoprecipitation (ChIP) protocol for studying histone modifications in Arabidopsis plants. Nature Protocols 3: 1018-1025. Schmittgen TD, Livak KJ. 2008. Analyzing real-time PCR data by the comparative CT method. Nature Protocols 3: 1101-1108. Shahmuradov IA, Umarov RK, Solovyev VV. 2017. TSSPlant: a new tool for prediction of plant Pol II promoters. Nucleic Acids Research 45: e65. Singh S, Kailasam S, Lo JC, Yeh KC. 2021. Histone H3 lysine4 trimethylation-regulated GRF11 expression is essential for the iron-deficiency response in Arabidopsis thaliana. New Phytologist 230: 244-258. Soler M, Plasencia A, Larbat R, Pouzet C, Jauneau A, Rivas S, Pesquet E, Lapierre C, Truchet I, Grima-Pettenati J. 2017. The Eucalyptus linker histone variant EgH1.3 cooperates with the transcription factor EgMYB1 to control lignin biosynthesis during wood formation. New Phytologist 213: 287-299. Stefanelli G, Azam AB, Walters BJ, Brimble MA, Gettens CP, Bouchard-Cannon P, Cheng HM, Davidoff AM, Narkaj K, Day JJ et al. 2018. Learning and age-related changes in genome-wide H2A.Z binding in the mouse hippocampus. Cell Reports 22: 1124-1131. Stroud H, Otero S, Desvoyes B, Ramirez-Parra E, Jacobsen SE, Gutierrez C. 2012. Genome-wide analysis of histone H3.1 and H3.3 variants in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 109: 5370-5375. Talbert PB, Henikoff S. 2021. Histone variants at a glance. Journal of Cell Science 134: jcs244749. Tenea GN, Spantzel J, Lee LY, Zhu Y, Lin K, Johnson SJ, Gelvin SB. 2009. Overexpression of several Arabidopsis histone genes increases agrobacterium-mediated transformation and transgene expression in plants. Plant Cell 21: 3350-3367. Vert G, Grotz N, Dedaldechamp F, Gaymard F, Guerinot ML, Briat JF, Curie C. 2002. IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell 14: 1223-1233. Wang HL, Yang Q, Tan S, Wang T, Zhang Y, Yang Y, Yin W, Xia X, Guo H, Li Z. 2022. Regulation of cytokinin biosynthesis using PtRD26pro-IPT module improves drought tolerance through PtARR10-PtYUC4/5-mediated reactive oxygen species removal in Populus. Journal of Integrative Plant Biology 64: 771-786. Wang HL, Zhang Y, Wang T, Yang Q, Yang Y, Li Z, Li B, Wen X, Li W, Yin W et al. 2021. An alternative splicing variant of PtRD26 delays leaf senescence by regulating multiple NAC transcription factors in Populus. Plant Cell 33: 1594-1614. Wang N, Cui Y, Liu Y, Fan H, Du J, Huang Z, Yuan Y, Wu H, Ling HQ. 2013. Requirement and functional redundancy of Ib subgroup bHLH proteins for iron deficiency responses and uptake in Arabidopsis thaliana. Molecular Plant 6: 503-513. Wang X, Gao J, Gao S, Song Y, Yang Z, Kuai B. 2019. The H3K27me3 demethylase REF6 promotes leaf senescence through directly activating major senescence regulatory and functional genes in Arabidopsis. PLoS Genetics 15: e1008068. Wollmann H, Holec S, Alden K, Clarke ND, Jacques PE, Berger F. 2012. Dynamic deposition of histone variant H3.3 accompanies developmental remodeling of the Arabidopsis transcriptome. PLoS Genetics 8: e1002658. Woo HR, Kim HJ, Lim PO, Nam HG. 2019. Leaf senescence: systems and dynamics aspects. Annual Review of Plant Biology 70: 347-376. Woo HR, Kim HJ, Nam HG, Lim PO. 2013. Plant leaf senescence and death - regulation by multiple layers of control and implications for aging in general. Journal of Cell Science 126(Pt 21): 4823-4833. Xing J, Wang T, Ni Z. 2015. Epigenetic regulation of iron homeostasis in Arabidopsis. Plant Signaling & Behavior 10: e1064574. Yan A, Borg M, Berger F, Chen Z. 2020. The atypical histone variant H3.15 promotes callus formation in Arabidopsis thaliana. Development 147: dev184895. Yang Y, Ou B, Zhang J, Si W, Gu H, Qin G, Qu LJ. 2014. The Arabidopsis mediator subunit MED16 regulates iron homeostasis by associating with EIN3/EIL1 through subunit MED25. The Plant Journal 77: 838-851. Yelagandula R, Stroud H, Holec S, Zhou K, Feng S, Zhong X, Muthurajan UM, Nie X, Kawashima T, Groth M et al. 2014. The histone variant H2A.W defines heterochromatin and promotes chromatin condensation in Arabidopsis. Cell 158: 98-109. Yi SJ, Kim K. 2020. New Insights into the role of histone changes in aging. International Journal of Molecular Sciences 21: 8241. Yi Y, Guerinot ML. 1996. Genetic evidence that induction of root Fe(III) chelate reductase activity is necessary for iron uptake under iron deficiency. The Plant Journal 10: 835-844. Yuan L, Wang D, Cao L, Yu N, Liu K, Guo Y, Gan S, Chen L. 2020. Regulation of leaf longevity by DML3-mediated DNA demethylation. Molecular Plant 13: 1149-1161. Yuan Y, Wu H, Wang N, Li J, Zhao W, Du J, Wang D, Ling HQ. 2008. FIT interacts with AtbHLH38 and AtbHLH39 in regulating iron uptake gene expression for iron homeostasis in Arabidopsis. Cell Research 18: 385-397. Zahraeifard S, Foroozani M, Sepehri A, Oh DH, Wang G, Mangu V, Chen B, Baisakh N, Dassanayake M, Smith AP. 2018. Rice H2A.Z negatively regulates genes responsive to nutrient starvation but promotes expression of key housekeeping genes. Journal of Experimental Botany 69: 4907-4919. Zhang J, Liu B, Li M, Feng D, Jin H, Wang P, Liu J, Xiong F, Wang J, Wang HB. 2015. The bHLH transcription factor bHLH104 interacts with IAA-LEUCINE RESISTANT3 and modulates iron homeostasis in Arabidopsis. Plant Cell 27: 787-805. Zhao F, Zhang H, Zhao T, Li Z, Jiang D. 2021. The histone variant H3.3 promotes the active chromatin state to repress flowering in Arabidopsis. Plant Physiology 186: 2051-2063. Zhou W, Zhu Y, Dong A, Shen WH. 2015. Histone H2A/H2B chaperones: from molecules to chromatin-based functions in plant growth and development. The Plant Journal 83: 78-95. Zuo J, Niu QW, Chua NH. 2000. Technical advance: an estrogen receptor-based transactivator XVE mediates highly inducible gene expression in transgenic plants. The Plant Journal 24: 265-273. |
فهرسة مساهمة: | Keywords: HTB4; histone variant; iron homeostasis; leaf senescence; transcription factor |
المشرفين على المادة: | 0 (Basic Helix-Loop-Helix Transcription Factors) 0 (Arabidopsis Proteins) 0 (Histones) 0 (Membrane Transport Proteins) 0 (bHLH101 protein, Arabidopsis) |
تواريخ الأحداث: | Date Created: 20230602 Date Completed: 20230922 Latest Revision: 20230924 |
رمز التحديث: | 20231215 |
DOI: | 10.1111/nph.19008 |
PMID: | 37265004 |
قاعدة البيانات: | MEDLINE |
تدمد: | 1469-8137 |
---|---|
DOI: | 10.1111/nph.19008 |