植物根尖干细胞的表观遗传调控
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摘要
干细胞是一类具有特化为不同细胞类型能力的多能性细胞,他为多细胞生物的器官发生、损伤修复和再生源源不断提供新细胞。干细胞的特化和维持需要复杂的基因调控网络来有序调控。此外,表观遗传调控在包括干细胞命运决定在内的许多生物学过程中发挥极其重要的作用。本文归纳了近年来对植物,主要是模式植物拟南芥(Arabidopsis thaliana (L.) Heynh.)根尖干细胞表观遗传调控方面的研究进展,重点论述了表观调控因子与控制干细胞的关键转录因子之间如何互作、调控植物根尖干细胞的自我更新和分化,并对今后研究的突破方向进行了展望。
Stem cells are a group of pluripotent cells that can differentiate into a diverse range of specialized cell types. They continuously provide new cells for organogenesis,wound repair,and regeneration in multicellular organisms. Stem cell specification and differentiation are orchestrated by complex gene regulatory networks. In addition,epigenetic regulation plays a crucial role in many biological events,including stem cell determination. In this review,we summarize recent advances in epigenetic control of root stem cells in the model plant Arabidopsis thaliana. Specifically,we focus on the interplay between epigenetic regulators and stem cell-controlling key transcription factors,which regulates root stem cell self-renewal and differentiation in plants.
Stem cells are a group of pluripotent cells that can differentiate into a diverse range of specialized cell types. They continuously provide new cells for organogenesis,wound repair,and regeneration in multicellular organisms. Stem cell specification and differentiation are orchestrated by complex gene regulatory networks. In addition,epigenetic regulation plays a crucial role in many biological events,including stem cell determination. In this review,we summarize recent advances in epigenetic control of root stem cells in the model plant Arabidopsis thaliana. Specifically,we focus on the interplay between epigenetic regulators and stem cell-controlling key transcription factors,which regulates root stem cell self-renewal and differentiation in plants.
引文
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[2]张倩倩，郑童，予茜，葛磊．生长素与植物根尖干细胞巢的维持[J]．植物学报，2018,53(1):126-138.Zhang QQ,Zheng T,Yu Q,Ge L. Auxin and the maintenance of root stem cell niches in plants[J]. Chinese Bulletin of Botany,2018,53(1):126-138.
[3] Berg CVD,Willemsen V,Hage W,Weisbeek P,Scheres B. Cell fate in the Arabidopsis root meristem determined by directional signalling[J]. Nature,1995,378(6552):62-65.
[4] Berg CVD, Willemsen V, Hendriks G, Weisbeek P,Scheres B. Short-range control of cell differentiation in the Arabidopsis root meristem[J]. Nature,1997,390(6657):287-289.
[5] Kouzarides T. Chromatin modifications and their function[J]. Cell,2007,128(4):693-705.
[6]胡惠雯，付莹．植物发育与表观遗传研究综述[J]．现代农业科技，2018(24):47-50.Hu HW,Fu Y. Review of plant development and epigenetics[J]. Modern Agricultural Sciences and Technology,2018(24):47-50.
[7] Henderson IR,Jacobsen SE. Epigenetic inheritance in plants[J]. Nature,2007,447(7143):418-424.
[8] Kawakatsu T,Stuart T,Valdes M,Breakfield N,Schmitz RJ,et al. Unique cell-type-specific patterns of DNA methy-lation in the root meristem[J]. Nat Plants,2016,2(5):e16058.
[9] Xiao W,Custard KD,Brown RC,Lemmon BE,Harada JJ,et al. DNA methylation is critical for Arabidopsis embryogenesis and seed viability[J]. Plant Cell,2006,18(4):805-814.
[10] Goldberg AD,Allis CD,Bernstein E. Epigenetics:a landscape takes shape[J]. Cell,2007,128(4):635-638.
[11] Kleff S,Andrulis ED,Anderson CW,Sternglanz R. Identification of a gene encoding a yeast histone H4 acetyltransferase[J]. J Biol Chem,1995,270(42):24674-24677.
[12] Kornet N, Scheres B. Members of the GCN5 histone acetyltransferase complex regulate PLETHORA-mediated root stem cell niche maintenance and transit amplifying cell proliferation in Arabidopsis[J]. Plant Cell,2009,21(4):1070-1079.
[13] Zhao Y,Cheng S,Song Y,Huang Y,Zhou S,et al. The interaction between rice ERF3 and WOX11 promotes crown root development by regulating gene expression involved in cytokinin signaling[J]. Plant Cell,2015,27(9):2469-2483.
[14] Nguyen HN,Kim JH,Jeong CY,Hong SW,Lee H. Inhibition of histone deacetylation alters Arabidopsis root growth in response to auxin via PIN1 degradation[J]. Plant Cell Rep,2013,32(10):1625-1636.
[15] Pi L,Aichinger E,Graaff E,Lavata PC,Weijers D,et al.Organizer-derived WOX5 signal maintains root columella stem cells through chromatin-mediated repression of CDF4expression[J]. Dev Cell,2015,33(5):576-588.
[16] Li H, Torres-Garcia J, Latrasse D, Benhamed M,Schilderink S,et al. Plant-specific histone deacetylases HDT1/2 regulate GIBBERELLIN 2-OXIDASE2 expression to control Arabidopsis root meristem cell number[J]. Plant Cell,2017,29(9):2183-2196.
[17] Hu YF,Qin FJ,Huang LM,Sun QW,Li C,et al. Rice histone deacetylase genes display specific expression patterns and developmental functions[J]. Biochem Biophys Res Commun,2009,388(2):266-271.
[18] Zhu Z,Xu F,Zhang Y,Cheng YT,Wiermer M,et al. Arabidopsis resistance protein SNC1 activates immune responses through association with a transcriptional corepressor[J]. Proc Natl Acad Sci USA,2010,107(31):13960-13965.
[19] Sarkar AK,Luijten M,Miyashima S,Lenhard M,Hashimoto T,et al. Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers[J].Nature,2007,446(7137):811-814.
[20] Berr A,McCallum EJ,Ménard R,Meyer D,Fuchs J,et al. Arabidopsis SET DOMAIN GROUP2 is required for H3K4 trimethylation and is crucial for both sporophyte and gametophyte development[J]. Plant Cell,2010,22(10):3232-3248.
[21] Yao X,Feng H,Yu Y,Dong A,Shen WH. SDG2-mediated H3K4 methylation is required for proper Arabidopsis root growth and development[J]. PLo S One,2013,8(2):e56537.
[22] Han P,Li Q,Zhu YX. Mutation of Arabidopsis BARD1causes meristem defects by failing to confine WUSCHEL expression to the organizing center[J]. Plant Cell,2008,20(6):1482-1493.
[23] Zhang Y,Jiao Y,Liu Z,Zhu YX. ROW1 maintains quiescent centre identity by confining WOX5 expression to specific cells[J]. Nat Commun,2015,6:6003.
[24] Kumpf R,Thorstensen T,Rahman MA,Heyman J,Nenseth HZ,et al. The ASH1-RELATED3 SET-domain protein controls cell division competence of the meristem and the quiescent center of the Arabidopsis primary root[J]. Plant Physiol,2014,166(2):632-643.
[25]胡博，金璐，周雅智，阮颖．植物Polycomb Group功能研究进展[J]．湖南农业科学，2014(9):9-11.Hu B,Jin L,Zhou YZ,Ruan Y. Advance in function of Polycomb Group in plants[J]. Hunan Agricultural Sciences,2014(9):9-11.
[26] Aichinger E,Villar CBR,Di Mambro R,Sabatini S,Khler C. The CHD3 chromatin remodeler PICKLE and Polycomb group proteins antagonistically regulate meristem activity in the Arabidopsis root[J]. Plant Cell,2011,23(3):1047-1060.
[27] De LM,Pu L,Turco GM,Gaudinier A,Marao AK,et al.Transcriptional regulation of Arabidopsis Polycomb Repressive Complex 2 coordinates cell-type proliferation and differentiation[J]. Plant Cell,2016,28(10):2616-2631.
[28] Hargreaves DC,Crabtree GR. ATP-dependent chromatin remodeling:genetics,genomics and mechanisms[J].Cell Res,2011,21(3):396-420.
[29] Choi KY,Yoo M,Han JH. Toward understanding the role of the neuron-specific BAF chromatin remodeling complex in memory formation[J]. Exp Mol Med,2015,47(4):e155.
[30] Shen WH,Xu L. Chromatin remodeling in stem cell maintenance in Arabidopsis thaliana[J]. Mol Plant,2009,2(4):600-609.
[31] Ogas J,Cheng JC,Sung ZR,Somerville C. Cellular differentiation regulated by gibberellin in the Arabidopsis thaliana pickle mutant[J]. Science,1997,277(5322):91-94.
[32] Ogas J,Kaufmann S,Henderson J,Somerville C. PICKLE is a CHD3 chromatin-remodeling factor that regulates the transition from embryonic to vegetative development in Arabidopsis[J]. Proc Natl Acad Sci USA,1999,96(24):13839-13844.
[33] Carter B,Bishop B,Ho KK,Huang R,Jia W,et al. The chromatin remodelers PKL and PIE1 act in an epigenetic pathway that determines H3K27me3 homeostasis in Arabidopsis[J]. Plant Cell,2018,30(6):1337-1352.
[34] Yang S,Li C,Zhao L,Gao S,Lu J,et al. The Arabidopsis SWI2/SNF2 chromatin remodeling ATPase BRAHMA targets directly to PINs and is required for root stem cell niche maintenance[J]. Plant Cell,2015,27(6):1670-1680.
[35] Kang H,Ma J,Wu D,Shen WH,Zhu Y. Functional coordination of the chromatin-remodeling factor At INO80 and the histone chaperones NRP1/2 in inflorescence meristem and root apical meristem[J]. Front Plant Sci,2019,10:115-125.
[36] Sang Y,Silvaortega CO,Wu S,Yamaguchi N,Wu MF,et al. Mutations in two non-canonical Arabidopsis SWI2/SNF2 chromatin remodeling ATPases cause embryogenesis and stem cell maintenance defects[J]. Plant J,2012,72(6):1000-1014.
[37] Cech TR,Steitz JA. The noncoding RNA revolution:trashing old rules to forge new ones[J]. Cell,2014,157(1):77-94.
[38] Gebert LFR,MacRae IJ. Regulation of microRNA function in animals[J]. Nat Rev Mol Cell Biol,2018,20:21-37.
[39] Wang JW,Wang LJ,Mao YB,Cai WJ,Xue HW,et al.Control of root cap formation by microRNA-targeted auxin response factors in Arabidopsis[J]. Plant Cell,2005,17(8):2204-2216.
[40] Ding Z,Friml J. Auxin regulates distal stem cell differentiation in Arabidopsis roots[J]. Proc Natl Acad Sci USA,2010,107(26):12046-12051.
[41] Grigg SP,Galinha C,Kornet N,Canales C,Scheres B,et al. Repression of apical homeobox genes is required for embryonic root development in Arabidopsis[J]. Curr Biol,2009,19(17):1485-1490.
[42] Smith ZR,Long JA. Control of Arabidopsis apical-basal embryo polarity by antagonistic transcription factors[J].Nature,2010,464(7287):423-426.
[43] Bazin J,Khan GA,Combier JP,Bustos-Sanmamed P,Debernardi JM,et al. MiR396 affects mycorrhization and root meristem activity in the legume Medicago truncatula[J]. Plant J,2013,74(6):920-934.
[44] Rodriguez RE,Ercoli MF,Debernardi JM,Breakfield NW,Mecchia MA,et al. MicroRNA miR396 regulates the switch between stem cells and transit-amplifying cells in Arabidopsis roots[J]. Plant Cell,2015,27(12):3354-3366.
[45] Ercoli MF,Rojas AML,Debernardi JM,Palatnik JF,Rodriguez RE. Control of cell proliferation and elongation by miR396[J]. Plant Signal Behav,2016,11(6):e1184809.
[46] Somssich M,Je BI,Simon R,Jackson D. CLAVATAWUSCHEL signaling in the shoot meristem[J]. Development,2016,143(18):3238-3248.
[2]张倩倩，郑童，予茜，葛磊．生长素与植物根尖干细胞巢的维持[J]．植物学报，2018,53(1):126-138.Zhang QQ,Zheng T,Yu Q,Ge L. Auxin and the maintenance of root stem cell niches in plants[J]. Chinese Bulletin of Botany,2018,53(1):126-138.
[3] Berg CVD,Willemsen V,Hage W,Weisbeek P,Scheres B. Cell fate in the Arabidopsis root meristem determined by directional signalling[J]. Nature,1995,378(6552):62-65.
[4] Berg CVD, Willemsen V, Hendriks G, Weisbeek P,Scheres B. Short-range control of cell differentiation in the Arabidopsis root meristem[J]. Nature,1997,390(6657):287-289.
[5] Kouzarides T. Chromatin modifications and their function[J]. Cell,2007,128(4):693-705.
[6]胡惠雯，付莹．植物发育与表观遗传研究综述[J]．现代农业科技，2018(24):47-50.Hu HW,Fu Y. Review of plant development and epigenetics[J]. Modern Agricultural Sciences and Technology,2018(24):47-50.
[7] Henderson IR,Jacobsen SE. Epigenetic inheritance in plants[J]. Nature,2007,447(7143):418-424.
[8] Kawakatsu T,Stuart T,Valdes M,Breakfield N,Schmitz RJ,et al. Unique cell-type-specific patterns of DNA methy-lation in the root meristem[J]. Nat Plants,2016,2(5):e16058.
[9] Xiao W,Custard KD,Brown RC,Lemmon BE,Harada JJ,et al. DNA methylation is critical for Arabidopsis embryogenesis and seed viability[J]. Plant Cell,2006,18(4):805-814.
[10] Goldberg AD,Allis CD,Bernstein E. Epigenetics:a landscape takes shape[J]. Cell,2007,128(4):635-638.
[11] Kleff S,Andrulis ED,Anderson CW,Sternglanz R. Identification of a gene encoding a yeast histone H4 acetyltransferase[J]. J Biol Chem,1995,270(42):24674-24677.
[12] Kornet N, Scheres B. Members of the GCN5 histone acetyltransferase complex regulate PLETHORA-mediated root stem cell niche maintenance and transit amplifying cell proliferation in Arabidopsis[J]. Plant Cell,2009,21(4):1070-1079.
[13] Zhao Y,Cheng S,Song Y,Huang Y,Zhou S,et al. The interaction between rice ERF3 and WOX11 promotes crown root development by regulating gene expression involved in cytokinin signaling[J]. Plant Cell,2015,27(9):2469-2483.
[14] Nguyen HN,Kim JH,Jeong CY,Hong SW,Lee H. Inhibition of histone deacetylation alters Arabidopsis root growth in response to auxin via PIN1 degradation[J]. Plant Cell Rep,2013,32(10):1625-1636.
[15] Pi L,Aichinger E,Graaff E,Lavata PC,Weijers D,et al.Organizer-derived WOX5 signal maintains root columella stem cells through chromatin-mediated repression of CDF4expression[J]. Dev Cell,2015,33(5):576-588.
[16] Li H, Torres-Garcia J, Latrasse D, Benhamed M,Schilderink S,et al. Plant-specific histone deacetylases HDT1/2 regulate GIBBERELLIN 2-OXIDASE2 expression to control Arabidopsis root meristem cell number[J]. Plant Cell,2017,29(9):2183-2196.
[17] Hu YF,Qin FJ,Huang LM,Sun QW,Li C,et al. Rice histone deacetylase genes display specific expression patterns and developmental functions[J]. Biochem Biophys Res Commun,2009,388(2):266-271.
[18] Zhu Z,Xu F,Zhang Y,Cheng YT,Wiermer M,et al. Arabidopsis resistance protein SNC1 activates immune responses through association with a transcriptional corepressor[J]. Proc Natl Acad Sci USA,2010,107(31):13960-13965.
[19] Sarkar AK,Luijten M,Miyashima S,Lenhard M,Hashimoto T,et al. Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers[J].Nature,2007,446(7137):811-814.
[20] Berr A,McCallum EJ,Ménard R,Meyer D,Fuchs J,et al. Arabidopsis SET DOMAIN GROUP2 is required for H3K4 trimethylation and is crucial for both sporophyte and gametophyte development[J]. Plant Cell,2010,22(10):3232-3248.
[21] Yao X,Feng H,Yu Y,Dong A,Shen WH. SDG2-mediated H3K4 methylation is required for proper Arabidopsis root growth and development[J]. PLo S One,2013,8(2):e56537.
[22] Han P,Li Q,Zhu YX. Mutation of Arabidopsis BARD1causes meristem defects by failing to confine WUSCHEL expression to the organizing center[J]. Plant Cell,2008,20(6):1482-1493.
[23] Zhang Y,Jiao Y,Liu Z,Zhu YX. ROW1 maintains quiescent centre identity by confining WOX5 expression to specific cells[J]. Nat Commun,2015,6:6003.
[24] Kumpf R,Thorstensen T,Rahman MA,Heyman J,Nenseth HZ,et al. The ASH1-RELATED3 SET-domain protein controls cell division competence of the meristem and the quiescent center of the Arabidopsis primary root[J]. Plant Physiol,2014,166(2):632-643.
[25]胡博，金璐，周雅智，阮颖．植物Polycomb Group功能研究进展[J]．湖南农业科学，2014(9):9-11.Hu B,Jin L,Zhou YZ,Ruan Y. Advance in function of Polycomb Group in plants[J]. Hunan Agricultural Sciences,2014(9):9-11.
[26] Aichinger E,Villar CBR,Di Mambro R,Sabatini S,Khler C. The CHD3 chromatin remodeler PICKLE and Polycomb group proteins antagonistically regulate meristem activity in the Arabidopsis root[J]. Plant Cell,2011,23(3):1047-1060.
[27] De LM,Pu L,Turco GM,Gaudinier A,Marao AK,et al.Transcriptional regulation of Arabidopsis Polycomb Repressive Complex 2 coordinates cell-type proliferation and differentiation[J]. Plant Cell,2016,28(10):2616-2631.
[28] Hargreaves DC,Crabtree GR. ATP-dependent chromatin remodeling:genetics,genomics and mechanisms[J].Cell Res,2011,21(3):396-420.
[29] Choi KY,Yoo M,Han JH. Toward understanding the role of the neuron-specific BAF chromatin remodeling complex in memory formation[J]. Exp Mol Med,2015,47(4):e155.
[30] Shen WH,Xu L. Chromatin remodeling in stem cell maintenance in Arabidopsis thaliana[J]. Mol Plant,2009,2(4):600-609.
[31] Ogas J,Cheng JC,Sung ZR,Somerville C. Cellular differentiation regulated by gibberellin in the Arabidopsis thaliana pickle mutant[J]. Science,1997,277(5322):91-94.
[32] Ogas J,Kaufmann S,Henderson J,Somerville C. PICKLE is a CHD3 chromatin-remodeling factor that regulates the transition from embryonic to vegetative development in Arabidopsis[J]. Proc Natl Acad Sci USA,1999,96(24):13839-13844.
[33] Carter B,Bishop B,Ho KK,Huang R,Jia W,et al. The chromatin remodelers PKL and PIE1 act in an epigenetic pathway that determines H3K27me3 homeostasis in Arabidopsis[J]. Plant Cell,2018,30(6):1337-1352.
[34] Yang S,Li C,Zhao L,Gao S,Lu J,et al. The Arabidopsis SWI2/SNF2 chromatin remodeling ATPase BRAHMA targets directly to PINs and is required for root stem cell niche maintenance[J]. Plant Cell,2015,27(6):1670-1680.
[35] Kang H,Ma J,Wu D,Shen WH,Zhu Y. Functional coordination of the chromatin-remodeling factor At INO80 and the histone chaperones NRP1/2 in inflorescence meristem and root apical meristem[J]. Front Plant Sci,2019,10:115-125.
[36] Sang Y,Silvaortega CO,Wu S,Yamaguchi N,Wu MF,et al. Mutations in two non-canonical Arabidopsis SWI2/SNF2 chromatin remodeling ATPases cause embryogenesis and stem cell maintenance defects[J]. Plant J,2012,72(6):1000-1014.
[37] Cech TR,Steitz JA. The noncoding RNA revolution:trashing old rules to forge new ones[J]. Cell,2014,157(1):77-94.
[38] Gebert LFR,MacRae IJ. Regulation of microRNA function in animals[J]. Nat Rev Mol Cell Biol,2018,20:21-37.
[39] Wang JW,Wang LJ,Mao YB,Cai WJ,Xue HW,et al.Control of root cap formation by microRNA-targeted auxin response factors in Arabidopsis[J]. Plant Cell,2005,17(8):2204-2216.
[40] Ding Z,Friml J. Auxin regulates distal stem cell differentiation in Arabidopsis roots[J]. Proc Natl Acad Sci USA,2010,107(26):12046-12051.
[41] Grigg SP,Galinha C,Kornet N,Canales C,Scheres B,et al. Repression of apical homeobox genes is required for embryonic root development in Arabidopsis[J]. Curr Biol,2009,19(17):1485-1490.
[42] Smith ZR,Long JA. Control of Arabidopsis apical-basal embryo polarity by antagonistic transcription factors[J].Nature,2010,464(7287):423-426.
[43] Bazin J,Khan GA,Combier JP,Bustos-Sanmamed P,Debernardi JM,et al. MiR396 affects mycorrhization and root meristem activity in the legume Medicago truncatula[J]. Plant J,2013,74(6):920-934.
[44] Rodriguez RE,Ercoli MF,Debernardi JM,Breakfield NW,Mecchia MA,et al. MicroRNA miR396 regulates the switch between stem cells and transit-amplifying cells in Arabidopsis roots[J]. Plant Cell,2015,27(12):3354-3366.
[45] Ercoli MF,Rojas AML,Debernardi JM,Palatnik JF,Rodriguez RE. Control of cell proliferation and elongation by miR396[J]. Plant Signal Behav,2016,11(6):e1184809.
[46] Somssich M,Je BI,Simon R,Jackson D. CLAVATAWUSCHEL signaling in the shoot meristem[J]. Development,2016,143(18):3238-3248.