Characterization of Transcriptome Remodeling during Cambium Formation Identifies and As Opposing Regulators of Secondary Growth
Cell-to-cell communication is crucial for the development of multicellular organisms, especially during the generation of new tissues and organs. Secondary growth—the lateral expansion of plant growth axes—is a highly dynamic process that depends on the activity of the cambium. The cambium is a stem cell–like tissue whose activity is responsible for wood production and, thus, for the establishment of extended shoot and root systems. Attempts to study cambium regulation at the molecular level have been hampered by the limitations of performing genetic analyses in trees and by the difficulty of accessing this tissue in model systems such as Arabidopsis thaliana. Here, we describe the roles of two receptor-like kinases, REDUCED IN LATERAL GROWTH1 (RUL1) and MORE LATERAL GROWTH1 (MOL1), as opposing regulators of cambium activity. Their identification was facilitated by a novel in vitro system in which cambium formation is induced in isolated Arabidopsis stem fragments. By combining this system with laser capture microdissection, we characterized transcriptome remodeling in a tissue- and stage-specific manner and identified series of genes induced during different phases of cambium formation. In summary, we provide a means for investigating cambium regulation in unprecedented depth and present two signaling components that control a process responsible for the accumulation of a large proportion of terrestrial biomass.
Vyšlo v časopise:
Characterization of Transcriptome Remodeling during Cambium Formation Identifies and As Opposing Regulators of Secondary Growth. PLoS Genet 7(2): e32767. doi:10.1371/journal.pgen.1001312
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1001312
Souhrn
Cell-to-cell communication is crucial for the development of multicellular organisms, especially during the generation of new tissues and organs. Secondary growth—the lateral expansion of plant growth axes—is a highly dynamic process that depends on the activity of the cambium. The cambium is a stem cell–like tissue whose activity is responsible for wood production and, thus, for the establishment of extended shoot and root systems. Attempts to study cambium regulation at the molecular level have been hampered by the limitations of performing genetic analyses in trees and by the difficulty of accessing this tissue in model systems such as Arabidopsis thaliana. Here, we describe the roles of two receptor-like kinases, REDUCED IN LATERAL GROWTH1 (RUL1) and MORE LATERAL GROWTH1 (MOL1), as opposing regulators of cambium activity. Their identification was facilitated by a novel in vitro system in which cambium formation is induced in isolated Arabidopsis stem fragments. By combining this system with laser capture microdissection, we characterized transcriptome remodeling in a tissue- and stage-specific manner and identified series of genes induced during different phases of cambium formation. In summary, we provide a means for investigating cambium regulation in unprecedented depth and present two signaling components that control a process responsible for the accumulation of a large proportion of terrestrial biomass.
Zdroje
1. AttaR
LaurensL
Boucheron-DubuissonE
Guivarc'hA
CarneroE
2009 Pluripotency of Arabidopsis xylem pericycle underlies shoot regeneration from root and hypocotyl explants grown in vitro. Plant J 57 626 644
2. CheP
LallS
NettletonD
HowellSH
2006 Gene expression programs during shoot, root, and callus development in Arabidopsis tissue culture. Plant Physiol 141 620 637
3. GrebT
ClarenzO
SchäferE
MüllerD
HerreroR
2003 Molecular analysis of the LATERAL SUPPRESSOR gene in Arabidopsis reveals a conserved control mechanism for axillary meristem formation. Genes Dev 17 1175 1187
4. SehrEM
AgustiJ
LehnerR
FarmerEE
SchwarzM
2010 Analysis of secondary growth in the Arabidopsis shoot reveals a positive role of jasmonate signalling in cambium formation. Plant J 63 811 822
5. DuJ
GrooverA
2010 Transcriptional regulation of secondary growth and wood formation. J Integr Plant Biol 52 17 27
6. FukakiH
Wysocka-DillerJ
KatoT
FujisawaH
BenfeyPN
1998 Genetic evidence that the endodermis is essential for shoot gravitropism in Arabidopsis thaliana. Plant J 14 425 430
7. AltamuraMM
PossentiM
MatteucciA
BaimaS
RubertiI
2001 Development of the vascular system in the inflorescence stem of Arabidopsis. New Phyt 151 381 389
8. SauerM
BallaJ
LuschnigC
WisniewskaJ
ReinohlV
2006 Canalization of auxin flow by Aux/IAA-ARF-dependent feedback regulation of PIN polarity. Genes Dev 20 2902 2911
9. EloA
ImmanenJ
NieminenK
HelariuttaY
2009 Stem cell function during plant vascular development. Semin Cell Dev Biol 20 1097 1106
10. SchraderJ
MoyleR
BhaleraoR
HertzbergM
LundebergJ
2004 Cambial meristem dormancy in trees involves extensive remodelling of the transcriptome. Plant J 40 173 187
11. LittleCHA
MacDonaldJE
OlssonO
2002 Involvement of indole-3-acetic acid in fascicular and interfascicular cambial growth and interfascicular extraxylary fiber differentiation in Arabidopsis thaliana inflorescence stems. International Journal of Plant Sciences 163 519 529
12. SchraderJ
BabaK
MayST
PalmeK
BennettM
2003 Polar auxin transport in the wood-forming tissues of hybrid aspen is under simultaneous control of developmental and environmental signals. Proc Natl Acad Sci U S A 100 10096 10101
13. DonnerTJ
SherrI
ScarpellaE
2009 Regulation of preprocambial cell state acquisition by auxin signaling in Arabidopsis leaves. Development 136 3235 3246
14. ScarpellaE
MarcosD
FrimlJ
BerlethT
2006 Control of leaf vascular patterning by polar auxin transport. Genes Dev 20 1015 1027
15. WenzelCL
SchuetzM
YuQ
MattssonJ
2007 Dynamics of MONOPTEROS and PIN-FORMED1 expression during leaf vein pattern formation in Arabidopsis thaliana. Plant J 49 387 398
16. SachsT
1981 The control of the patterned differentiation of vascular tissues. Adv Bot Res 9 151 162
17. EhltingJ
MattheusN
AeschlimanDS
LiE
HambergerB
2005 Global transcript profiling of primary stems from Arabidopsis thaliana identifies candidate genes for missing links in lignin biosynthesis and transcriptional regulators of fiber differentiation. Plant J 42 618 640
18. KoJH
HanKH
2004 Arabidopsis whole-transcriptome profiling defines the features of coordinated regulations that occur during secondary growth. Plant Mol Biol 55 433 453
19. KoJH
HanKH
ParkS
YangJ
2004 Plant body weight-induced secondary growth in Arabidopsis and its transcription phenotype revealed by whole-transcriptome profiling. Plant Physiol 135 1069 1083
20. OhS
ParkS
HanKH
2003 Transcriptional regulation of secondary growth in Arabidopsis thaliana. J Exp Bot 54 2709 2722
21. ZhaoC
CraigJC
PetzoldHE
DickermanAW
BeersEP
2005 The xylem and phloem transcriptomes from secondary tissues of the Arabidopsis root-hypocotyl. Plant Physiol 138 803 818
22. SchraderJ
NilssonJ
MellerowiczE
BerglundA
NilssonP
2004 A high-resolution transcript profile across the wood-forming meristem of poplar identifies potential regulators of cambial stem cell identity. Plant Cell 16 2278 2292
23. GrooverAT
MansfieldSD
DiFazioSP
DupperG
FontanaJR
2006 The Populus homeobox gene ARBORKNOX1 reveals overlapping mechanisms regulating the shoot apical meristem and the vascular cambium. Plant Mol Biol 61 917 932
24. FisherK
TurnerS
2007 PXY, a Receptor-like Kinase Essential for Maintaining Polarity during Plant Vascular-Tissue Development. Curr Biol 17 1061 1066
25. HirakawaY
ShinoharaH
KondoY
InoueA
NakanomyoI
2008 Non-cell-autonomous control of vascular stem cell fate by a CLE peptide/receptor system. Proc Natl Acad Sci U S A 105 15208 15213
26. EtchellsJP
TurnerSR
2010 The PXY-CLE41 receptor ligand pair defines a multifunctional pathway that controls the rate and orientation of vascular cell division. Development 137 767 774
27. De SmetI
VossU
JurgensG
BeeckmanT
2009 Receptor-like kinases shape the plant. Nat Cell Biol 11 1166 1173
28. JiJ
StrableJ
ShimizuR
KoenigD
SinhaN
2009 WOX4 promotes procambial development. Plant Physiol 152 1346 1356
29. HirakawaY
KondoY
FukudaH
2010 TDIF peptide signaling regulates vascular stem cell proliferation via the WOX4 homeobox gene in Arabidopsis. Plant Cell 22 2618 2629
30. MayerKF
SchoofH
HaeckerA
LenhardM
JurgensG
1998 Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95 805 815
31. SarkarAK
LuijtenM
MiyashimaS
LenhardM
HashimotoT
2007 Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446 811 814
32. KerkNM
CeseraniT
TaustaSL
SussexIM
NelsonTM
2003 Laser capture microdissection of cells from plant tissues. Plant Physiol 132 27 35
33. AgustiJ
MereloP
CercosM
TadeoFR
TalonM
2009 Comparative transcriptional survey between laser-microdissected cells from laminar abscission zone and petiolar cortical tissue during ethylene-promoted abscission in citrus leaves. BMC Plant Biol 9 127
34. JiaoY
TaustaSL
GandotraN
SunN
LiuT
2009 A transcriptome atlas of rice cell types uncovers cellular, functional and developmental hierarchies. Nat Genet 41 258 263
35. ZhangX
MadiS
BorsukL
NettletonD
ElshireRJ
2007 Laser microdissection of narrow sheath mutant maize uncovers novel gene expression in the shoot apical meristem. PLoS Genet 3 e101 doi:10.1371/journal.pgen.0030101
36. BradySM
OrlandoDA
LeeJY
WangJY
KochJ
2007 A high-resolution root spatiotemporal map reveals dominant expression patterns. Science 318 801 806
37. YadavRK
GirkeT
PasalaS
XieM
ReddyGV
2009 Gene expression map of the Arabidopsis shoot apical meristem stem cell niche. Proc Natl Acad Sci U S A 106 4941 4946
38. ChatfieldSP
StirnbergP
FordeBG
LeyserO
2000 The hormonal regulation of axillary bud growth in Arabidopsis. Plant J 24 159 169
39. FrimlJ
VietenA
SauerM
WeijersD
SchwarzH
2003 Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426 147 153
40. BonkeM
ThitamadeeS
MähönenAP
HauserMT
HelariuttaY
2003 APL regulates vascular tissue identity in Arabidopsis. Nature 426 181 186
41. TruernitE
BaubyH
DubreucqB
GrandjeanO
RunionsJ
2008 High-resolution whole-mount imaging of three-dimensional tissue organization and gene expression enables the study of Phloem development and structure in Arabidopsis. Plant Cell 20 1494 1503
42. NilssonJ
KarlbergA
AnttiH
Lopez-VernazaM
MellerowiczE
2008 Dissecting the molecular basis of the regulation of wood formation by auxin in hybrid aspen. Plant Cell 20 843 855
43. ScarpellaE
FrancisP
BerlethT
2004 Stage-specific markers define early steps of procambium development in Arabidopsis leaves and correlate termination of vein formation with mesophyll differentiation. Development 131 3445 3455
44. DevicM
2008 The importance of being essential: EMBRYO-DEFECTIVE genes in Arabidopsis. C R Biol 331 726 736
45. KwakSH
ShenR
SchiefelbeinJ
2005 Positional signaling mediated by a receptor-like kinase in Arabidopsis. Science 307 1111 1113
46. GeorgeL
RomanowskySM
HarperJF
SharrockRA
2008 The ACA10 Ca2+-ATPase regulates adult vegetative development and inflorescence architecture in Arabidopsis. Plant Physiol 146 716 728
47. LinPC
HwangSG
EndoA
OkamotoM
KoshibaT
2007 Ectopic expression of ABSCISIC ACID 2/GLUCOSE INSENSITIVE 1 in Arabidopsis promotes seed dormancy and stress tolerance. Plant Physiol 143 745 758
48. DongCH
RivarolaM
ResnickJS
MagginBD
ChangC
2008 Subcellular co-localization of Arabidopsis RTE1 and ETR1 supports a regulatory role for RTE1 in ETR1 ethylene signaling. Plant J 53 275 286
49. ZhangJ
EloA
HelariuttaY
2010 Arabidopsis as a model for wood formation. Curr Opin Biotechnol Epub ahead of print
50. GrooverAT
2005 What genes make a tree a tree? Trends Plant Sci 10 210 214
51. QinY
LeydonAR
ManzielloA
PandeyR
MountD
2009 Penetration of the stigma and style elicits a novel transcriptome in pollen tubes, pointing to genes critical for growth in a pistil. PLoS Genet 5 e1000621 doi:10.1371/journal.pgen.1000621
52. SauerM
FrimlJ
2008 In vitro culture of Arabidopsis embryos. Methods Mol Biol 427 71 76
53. SnowR
1935 Activation of cambial growth by pure hormones. New Phyt 34 347 360
54. BjörklundS
AnttiH
UddestrandI
MoritzT
SundbergB
2007 Cross-talk between gibberellin and auxin in development of Populus wood: gibberellin stimulates polar auxin transport and has a common transcriptome with auxin. Plant J 52 499 511
55. LauxT
MayerKF
BergerJ
JurgensG
1996 The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development 122 87 96
56. ShiuSH
KarlowskiWM
PanR
TzengYH
MayerKF
2004 Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell 16 1220 1234
57. StahlY
WinkRH
IngramGC
SimonR
2009 A signaling module controlling the stem cell niche in Arabidopsis root meristems. Curr Biol 19 909 914
58. SchoofH
LenhardM
HaeckerA
MayerKF
JurgensG
2000 The stem cell population of Arabidopsis shoot meristems in maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100 635 644
59. MelzerS
LensF
GennenJ
VannesteS
RohdeA
2008 Flowering-time genes modulate meristem determinacy and growth form in Arabidopsis thaliana. Nature Genetics 40 1489 1492
60. KwakSH
Schiefelbein J 2008 A feedback mechanism controlling SCRAMBLED receptor accumulation and cell-type pattern in Arabidopsis. Curr Biol 18 1949 1954
61. DeYoungBJ
BickleKL
SchrageKJ
MuskettP
PatelK
2006 The CLAVATA1-related BAM1, BAM2 and BAM3 receptor kinase-like proteins are required for meristem function in Arabidopsis. Plant J 45 1 16
62. ZhuY
WangY
LiR
SongX
WangQ
2010 Analysis of interactions among the CLAVATA3 receptors reveals a direct interaction between CLAVATA2 and CORYNE in Arabidopsis. Plant J 61 223 233
63. GuoY
HanL
HymesM
DenverR
ClarkSE
2010 CLAVATA2 forms a distinct CLE-binding receptor complex regulating Arabidopsis stem cell specification. Plant J 23 889 900
64. BleckmannA
Weidtkamp-PetersS
SeidelCA
SimonR
2010 Stem cell signaling in Arabidopsis requires CRN to localize CLV2 to the plasma membrane. Plant Physiol 152 166 176
65. SolomonBD
2010 Biofuels and sustainability. Ann N Y Acad Sci 1185 119 134
66. GentlemanRC
CareyVJ
BatesDM
BolstadB
DettlingM
2004 Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5 R80
67. BarrettT
TroupDB
WilhiteSE
LedouxP
RudnevD
2009 NCBI GEO: archive for high-throughput functional genomic data. Nucleic Acids Research 37 D885 890
68. LarkinMA
BlackshieldsG
BrownNP
ChennaR
McGettiganPA
2007 Clustal W and Clustal X version 2.0. Bioinformatics 23 2947 2948
69. SaitouN
NeiM
1987 The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4 406 425
70. KimuraM
1983 The neutral Theory of Molecular Evolution. Cambridge Camb.Univ.Press 75
71. HwangI
ChenHC
SheenJ
2002 Two-component signal transduction pathways in Arabidopsis. Plant Physiol 129 500 515
72. AkamaK
JunkerV
BeierH
2000 Identification of two catalytic subunits of tRNA splicing endonuclease from Arabidopsis thaliana. Gene 257 177 185
73. ZilbermanD
CaoX
JacobsenSE
2003 ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science 299 716 719
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