The BOP-type co-transcriptional regulator NODULE ROOT1 promotes stem secondary growth of the tropical Cannabaceae tree Parasponia andersonii.


Journal

The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397

Informations de publication

Date de publication:
06 2021
Historique:
received: 14 07 2020
accepted: 16 03 2021
pubmed: 19 3 2021
medline: 15 12 2021
entrez: 18 3 2021
Statut: ppublish

Résumé

Tree stems undergo a massive secondary growth in which secondary xylem and phloem tissues arise from the vascular cambium. Vascular cambium activity is driven by endogenous developmental signalling cues and environmental stimuli. Current knowledge regarding the genetic regulation of cambium activity and secondary growth is still far from complete. The tropical Cannabaceae tree Parasponia andersonii is a non-legume research model of nitrogen-fixing root nodulation. Parasponia andersonii can be transformed efficiently, making it amenable for CRISPR-Cas9-mediated reverse genetics. We considered whether P. andersonii also could be used as a complementary research system to investigate tree-related traits, including secondary growth. We established a developmental map of stem secondary growth in P. andersonii plantlets. Subsequently, we showed that the expression of the co-transcriptional regulator PanNODULE ROOT1 (PanNOOT1) is essential for controlling this process. PanNOOT1 is orthologous to Arabidopsis thaliana BLADE-ON-PETIOLE1 (AtBOP1) and AtBOP2, which are involved in the meristem-to-organ-boundary maintenance. Moreover, in species forming nitrogen-fixing root nodules, NOOT1 is known to function as a key nodule identity gene. Parasponia andersonii CRISPR-Cas9 loss-of-function Pannoot1 mutants are altered in the development of the xylem and phloem tissues without apparent disturbance of the cambium organization and size. Transcriptomic analysis showed that the expression of key secondary growth-related genes is significantly down-regulated in Pannoot1 mutants. This allows us to conclude that PanNOOT1 positively contributes to the regulation of stem secondary growth. Our work also demonstrates that P. andersonii can serve as a tree research system.

Identifiants

pubmed: 33735477
doi: 10.1111/tpj.15242
pmc: PMC9543857
doi:

Substances chimiques

Plant Proteins 0
Nitrogen N762921K75

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1366-1386

Informations de copyright

© 2021 The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd.

Références

Plant Cell Physiol. 2004 Oct;45(10):1361-70
pubmed: 15564519
Elife. 2014 Feb 11;3:e01567
pubmed: 24520159
Genes Dev. 2005 Aug 15;19(16):1855-60
pubmed: 16103214
Plant Physiol. 2010 Mar;152(3):1346-56
pubmed: 20044450
Plant J. 2009 Dec;60(6):1000-14
pubmed: 19737362
PLoS One. 2011 Feb 28;6(2):e17458
pubmed: 21386988
Plant Mol Biol. 2000 Nov;44(5):619-34
pubmed: 11198423
Plant Cell Rep. 2010 Mar;29(3):211-21
pubmed: 20087597
Plant Physiol. 2015 Nov;169(3):2166-86
pubmed: 26417006
New Phytol. 2020 Apr;226(2):541-554
pubmed: 31863481
J Exp Bot. 2017 Jan;68(1):27-43
pubmed: 27965363
J Vis Exp. 2014 May 13;(87):
pubmed: 24894795
New Phytol. 2017 Jul;215(2):642-657
pubmed: 28609015
Commun Biol. 2019 Jun 21;2:238
pubmed: 31263782
Proc Natl Acad Sci U S A. 2020 Mar 3;117(9):5059-5066
pubmed: 32041869
Plant Physiol. 2020 Oct;184(2):1004-1023
pubmed: 32669419
Plant Cell. 2012 Nov;24(11):4498-510
pubmed: 23136374
Elife. 2017 Aug 22;6:
pubmed: 28826468
Int J Mol Sci. 2019 Jul 24;20(15):
pubmed: 31344908
Plant Mol Biol. 2006 Aug;61(6):917-32
pubmed: 16927204
Development. 2008 Apr;135(8):1537-46
pubmed: 18339677
Plant Cell. 2007 Jan;19(1):270-80
pubmed: 17237351
Plant Biotechnol J. 2018 Mar;16(3):808-817
pubmed: 28905477
Plant Physiol. 2010 Jul;153(3):906-14
pubmed: 20488898
Plant Cell. 2004 Sep;16(9):2278-92
pubmed: 15316113
Plant Cell Rep. 2000 Jan;19(3):315-320
pubmed: 30754915
Trends Plant Sci. 2014 Dec;19(12):757-63
pubmed: 25239777
Nat Methods. 2017 Jul;14(7):687-690
pubmed: 28581496
Plant Cell. 1992 Oct;4(10):1199-211
pubmed: 1446169
Curr Biol. 2015 Apr 20;25(8):1050-5
pubmed: 25866390
Plant Cell. 2005 Jan;17(1):61-76
pubmed: 15598805
Physiol Plant. 2014 Jun;151(2):134-41
pubmed: 24053438
New Phytol. 2017 Mar;213(4):1697-1709
pubmed: 27891614
Development. 2010 Mar;137(5):767-74
pubmed: 20147378
Nat Biotechnol. 2016 May;34(5):525-7
pubmed: 27043002
Plant J. 2018 Jun;94(5):880-894
pubmed: 29570881
Curr Biol. 2008 Mar 25;18(6):458-63
pubmed: 18356049
Plant Signal Behav. 2016 Jun 2;11(6):e1191734
pubmed: 27232947
Science. 2011 Feb 18;331(6019):909-12
pubmed: 21205637
Plant Cell Physiol. 2010 Jun;51(6):1084-90
pubmed: 20427511
Curr Biol. 2007 Jun 19;17(12):1061-6
pubmed: 17570668
Proc Natl Acad Sci U S A. 2008 Sep 30;105(39):15208-13
pubmed: 18812507
Proc Natl Acad Sci U S A. 2018 May 15;115(20):E4700-E4709
pubmed: 29717040
Plant Mol Biol. 2006 Apr;60(6):915-28
pubmed: 16724261
Development. 2010 Mar;137(6):975-84
pubmed: 20179097
PLoS One. 2013 Jul 29;8(7):e69219
pubmed: 23922694
Science. 2006 Aug 11;313(5788):842-5
pubmed: 16902140
PLoS Genet. 2011 Feb;7(2):e1001312
pubmed: 21379334
Development. 2005 May;132(9):2203-13
pubmed: 15800002
Plant Cell. 2011 Sep;23(9):3247-59
pubmed: 21926336
Plant Cell. 2010 Jan;22(1):62-76
pubmed: 20118228
Bioresour Technol. 2010 Mar;101(6):1892-8
pubmed: 19914825
Front Plant Sci. 2018 Mar 06;9:284
pubmed: 29559988
Plant Physiol. 2010 Feb;152(2):1044-55
pubmed: 19965968
New Phytol. 2015 Dec;208(4):1149-56
pubmed: 26192091
Physiol Plant. 2002 Apr;114(4):594-600
pubmed: 11975734
Development. 2014 Nov;141(22):4311-9
pubmed: 25371365
Plant Cell. 2005 May;17(5):1434-48
pubmed: 15805484
Plant Physiol. 2016 Jun;171(2):1113-27
pubmed: 27208226
Plant Physiol. 1990 Jul;93(3):1110-6
pubmed: 16667565
Front Plant Sci. 2015 Dec 09;6:1052
pubmed: 26697027
Plant Cell. 2011 Apr;23(4):1322-36
pubmed: 21498678
New Phytol. 2016 Jan;209(1):228-40
pubmed: 26390061
EMBO J. 2013 Jan 23;32(2):178-93
pubmed: 23169537
Plant Cell. 2020 Jun;32(6):1868-1885
pubmed: 32276984
Plant J. 2016 May;86(3):210-20
pubmed: 26991973
Semin Cell Dev Biol. 2018 Jul;79:58-67
pubmed: 28864343
Sci Rep. 2017 Jun 1;7(1):2638
pubmed: 28572673
Nat Commun. 2019 Feb 6;10(1):619
pubmed: 30728357
Plant Biotechnol J. 2017 Oct;15(10):1309-1321
pubmed: 28258966
Plant Physiol. 1997 Oct;115(2):577-585
pubmed: 12223825
Nature. 2010 May 20;465(7296):316-21
pubmed: 20410882
Proc Natl Acad Sci U S A. 2017 Oct 10;114(41):E8656-E8664
pubmed: 28973898
ACS Synth Biol. 2014 Nov 21;3(11):839-43
pubmed: 24933124
Plant Cell. 2010 Aug;22(8):2618-29
pubmed: 20729381
J Vis Exp. 2019 Aug 18;(150):
pubmed: 31475981
Planta. 2017 Jun;245(6):1079-1090
pubmed: 28204875
Plant Cell. 2019 Jan;31(1):68-83
pubmed: 30610167
Plant Cell. 2007 Jun;19(6):1809-25
pubmed: 17601823
Development. 2013 May;140(10):2224-34
pubmed: 23578929
Arabidopsis Book. 2015 May 21;13:e0177
pubmed: 26078728
Plant Biotechnol J. 2019 Jan;17(1):206-219
pubmed: 29851301
Mol Plant. 2016 Oct 10;9(10):1406-1414
pubmed: 27449136
Science. 2006 Sep 15;313(5793):1596-604
pubmed: 16973872
Plant Sci. 2016 Nov;252:239-245
pubmed: 27717460
Protoplasma. 2014 Sep;251(5):1125-39
pubmed: 24526327
Curr Biol. 2016 Aug 8;26(15):1990-1997
pubmed: 27426519
Plant Biotechnol J. 2020 Jan;18(1):195-206
pubmed: 31199056
Plant Sci. 2014 Feb;215-216:157-71
pubmed: 24388527
Biotechnology (N Y). 1991 Oct;9(10):963-7
pubmed: 1368724
Plant J. 2020 Jul;103(2):645-659
pubmed: 32343459
Plant Cell. 2017 Jul;29(7):1585-1604
pubmed: 28655750
Dev Biol. 2010 May 1;341(1):95-113
pubmed: 19961843
Curr Opin Plant Biol. 2014 Feb;17:116-25
pubmed: 24507503
Plant Cell Rep. 2007 Sep;26(9):1529-38
pubmed: 17492451
Plant Cell. 2010 Oct;22(10):3461-73
pubmed: 20952636
New Phytol. 2019 Jun;222(4):1816-1831
pubmed: 30724367
Curr Opin Plant Biol. 2006 Feb;9(1):72-7
pubmed: 16337829
Plant Cell. 2006 Nov;18(11):3158-70
pubmed: 17114348
Plant Mol Biol. 2001 Sep;47(1-2):239-74
pubmed: 11554475
Plant Physiol. 2015 May;168(1):164-74
pubmed: 25818702
Plant Physiol. 2012 Feb;158(2):946-60
pubmed: 22114095
BMC Plant Biol. 2019 Dec 19;19(1):571
pubmed: 31856724
Nature. 2003 Nov 13;426(6963):181-6
pubmed: 14614507
Development. 2003 Jan;130(1):161-72
pubmed: 12441300
Plant Cell. 2008 Apr;20(4):843-55
pubmed: 18424614
Plant J. 2015 Jun;82(5):887-98
pubmed: 25903933
Genome Biol. 2015 Aug 06;16:157
pubmed: 26243257
Proc Natl Acad Sci U S A. 2013 Jun 25;110(26):10848-53
pubmed: 23754401
Nucleic Acids Res. 2014 Jan;42(Database issue):D1182-7
pubmed: 24174544
New Phytol. 2016 Jan;209(2):485-98
pubmed: 26391543
Annu Rev Plant Biol. 2019 Apr 29;70:293-319
pubmed: 30822110
Proc Natl Acad Sci U S A. 2008 Nov 25;105(47):18625-30
pubmed: 19011104
Bioinformatics. 2019 Nov 1;35(22):4779-4781
pubmed: 31199463

Auteurs

Defeng Shen (D)

Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University & Research, Wageningen, 6708PB, The Netherlands.

Rens Holmer (R)

Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University & Research, Wageningen, 6708PB, The Netherlands.

Olga Kulikova (O)

Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University & Research, Wageningen, 6708PB, The Netherlands.

Chanaka Mannapperuma (C)

Department of Plant Physiology, Umeå Plant Science Centre, Umeå University, Umeå, 907 36, Sweden.

Nathaniel R Street (NR)

Department of Plant Physiology, Umeå Plant Science Centre, Umeå University, Umeå, 907 36, Sweden.

Zhichun Yan (Z)

Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University & Research, Wageningen, 6708PB, The Netherlands.

Thomas van der Maden (T)

Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University & Research, Wageningen, 6708PB, The Netherlands.

Fengjiao Bu (F)

Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University & Research, Wageningen, 6708PB, The Netherlands.

Yuanyuan Zhang (Y)

Laboratory of Plant Physiology, Department of Plant Sciences, Wageningen University & Research, Wageningen, 6708 PB, The Netherlands.

Rene Geurts (R)

Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University & Research, Wageningen, 6708PB, The Netherlands.

Kévin Magne (K)

Laboratory of Molecular Biology, Department of Plant Sciences, Wageningen University & Research, Wageningen, 6708PB, The Netherlands.

Articles similaires

Amaryllidaceae Alkaloids Lycoris NADPH-Ferrihemoprotein Reductase Gene Expression Regulation, Plant Plant Proteins
Drought Resistance Gene Expression Profiling Gene Expression Regulation, Plant Gossypium Multigene Family
Animals Natural Killer T-Cells Mice Adipose Tissue Lipid Metabolism
India Carbon Sequestration Environmental Monitoring Carbon Biomass

Classifications MeSH