Gene expression underlying floral epidermal specialization in Aristolochia fimbriata (Aristolochiaceae).
Aristolochia
Piperales
epidermis development
multicellular trichomes
perianth
petaloid sepals
Journal
Annals of botany
ISSN: 1095-8290
Titre abrégé: Ann Bot
Pays: England
ID NLM: 0372347
Informations de publication
Date de publication:
07 05 2021
07 05 2021
Historique:
received:
16
10
2020
accepted:
22
02
2021
pubmed:
26
2
2021
medline:
26
5
2021
entrez:
25
2
2021
Statut:
ppublish
Résumé
The epidermis constitutes the outermost tissue of the plant body. Although it plays major structural, physiological and ecological roles in embryophytes, the molecular mechanisms controlling epidermal cell fate, differentiation and trichome development have been scarcely studied across angiosperms, and remain almost unexplored in floral organs. In this study, we assess the spatio-temporal expression patterns of GL2, GL3, TTG1, TRY, MYB5, MYB6, HDG2, MYB106-like, WIN1 and RAV1-like homologues in the magnoliid Aristolochia fimbriata (Aristolochiaceae) by using comparative RNA-sequencing and in situ hybridization assays. Genes involved in Aristolochia fimbriata trichome development vary depending on the organ where they are formed. Stem, leaf and pedicel trichomes recruit most of the transcription factors (TFs) described above. Conversely, floral trichomes only use a small subset of genes including AfimGL2, AfimRAV1-like, AfimWIN1, AfimMYB106-like and AfimHDG2. The remaining TFs, AfimTTG1, AfimGL3, AfimTRY, AfimMYB5 and AfimMYB6, are restricted to the abaxial (outer) and the adaxial (inner) pavement epidermal cells. We re-evaluate the core genetic network shaping trichome fate in flowers of an early-divergent angiosperm lineage and show a morphologically diverse output with a simpler genetic mechanism in place when compared to the models Arabidopsis thaliana and Cucumis sativus. In turn, our results strongly suggest that the canonical trichome gene expression appears to be more conserved in vegetative than in floral tissues across angiosperms.
Sections du résumé
BACKGROUND AND AIMS
The epidermis constitutes the outermost tissue of the plant body. Although it plays major structural, physiological and ecological roles in embryophytes, the molecular mechanisms controlling epidermal cell fate, differentiation and trichome development have been scarcely studied across angiosperms, and remain almost unexplored in floral organs.
METHODS
In this study, we assess the spatio-temporal expression patterns of GL2, GL3, TTG1, TRY, MYB5, MYB6, HDG2, MYB106-like, WIN1 and RAV1-like homologues in the magnoliid Aristolochia fimbriata (Aristolochiaceae) by using comparative RNA-sequencing and in situ hybridization assays.
KEY RESULTS
Genes involved in Aristolochia fimbriata trichome development vary depending on the organ where they are formed. Stem, leaf and pedicel trichomes recruit most of the transcription factors (TFs) described above. Conversely, floral trichomes only use a small subset of genes including AfimGL2, AfimRAV1-like, AfimWIN1, AfimMYB106-like and AfimHDG2. The remaining TFs, AfimTTG1, AfimGL3, AfimTRY, AfimMYB5 and AfimMYB6, are restricted to the abaxial (outer) and the adaxial (inner) pavement epidermal cells.
CONCLUSIONS
We re-evaluate the core genetic network shaping trichome fate in flowers of an early-divergent angiosperm lineage and show a morphologically diverse output with a simpler genetic mechanism in place when compared to the models Arabidopsis thaliana and Cucumis sativus. In turn, our results strongly suggest that the canonical trichome gene expression appears to be more conserved in vegetative than in floral tissues across angiosperms.
Identifiants
pubmed: 33630993
pii: 6149920
doi: 10.1093/aob/mcab033
pmc: PMC8103811
doi:
Substances chimiques
Arabidopsis Proteins
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
749-764Informations de copyright
© The Author(s) 2021. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.
Références
Development. 2008 Apr;135(7):1335-45
pubmed: 18305006
Front Plant Sci. 2015 Dec 11;6:1095
pubmed: 26697047
Plant J. 2009 Jul;59(1):52-62
pubmed: 19309462
J Exp Bot. 2000 Mar;51(344):497-505
pubmed: 10938806
Plant J. 1996 Sep;10(3):393-402
pubmed: 8811855
Curr Opin Plant Biol. 2009 Oct;12(5):587-92
pubmed: 19783469
Curr Opin Plant Biol. 2001 Oct;4(5):447-56
pubmed: 11597504
BMC Genomics. 2015 Oct 26;16:868
pubmed: 26503424
Development. 2003 Dec;130(26):6431-9
pubmed: 14627722
Hereditas. 2002;136(3):219-26
pubmed: 12471669
Syst Biol. 2008 Oct;57(5):758-71
pubmed: 18853362
Dev Biol. 1994 Dec;166(2):740-54
pubmed: 7813791
Mutat Res. 1982 Mar;93(1):109-23
pubmed: 7062928
Mol Plant. 2009 Jul;2(4):803-822
pubmed: 19626137
Plant Cell Physiol. 2006 Jan;47(1):107-27
pubmed: 16278222
Plant Physiol. 2016 Mar;170(3):1624-39
pubmed: 26802039
Cell. 1991 Nov 1;67(3):483-93
pubmed: 1934056
Cell Mol Life Sci. 2013 Jun;70(11):1937-48
pubmed: 22996257
Nucleic Acids Res. 2002 Jul 15;30(14):3059-66
pubmed: 12136088
Development. 2013 May;140(9):1924-35
pubmed: 23515473
Development. 2003 Oct;130(20):4859-69
pubmed: 12917293
J Exp Bot. 2014 Sep;65(17):4943-58
pubmed: 24962999
Cell. 1994 Feb 11;76(3):555-66
pubmed: 8313475
Development. 1999 Feb;126(4):671-82
pubmed: 9895315
Plant Cell. 1998 Dec;10(12):2047-62
pubmed: 9836744
Ann Bot. 2004 Jan;93(1):3-11
pubmed: 14678941
Development. 1998 Sep;125(17):3497-508
pubmed: 9693152
Front Plant Sci. 2018 Jun 20;9:840
pubmed: 29973945
Development. 2005 Jan;132(2):291-8
pubmed: 15590742
Nat Biotechnol. 2016 May;34(5):525-7
pubmed: 27043002
Mol Cell. 2000 Mar;5(3):569-79
pubmed: 10882141
Nature. 1994 Jun 23;369(6482):661-4
pubmed: 8208293
New Phytol. 2009 Aug;183(3):718-728
pubmed: 19659588
J Exp Bot. 2018 Apr 9;69(8):1887-1902
pubmed: 29438529
Plant Cell. 2009 Jan;21(1):72-89
pubmed: 19136646
Development. 2005 Apr;132(7):1477-85
pubmed: 15728674
Development. 1996 Mar;122(3):997-1005
pubmed: 8631276
Mol Syst Biol. 2008;4:217
pubmed: 18766177
Genomics. 2015 May;105(5-6):296-303
pubmed: 25666662
Development. 2005 Jan;132(2):359-70
pubmed: 15604096
Development. 2007 Nov;134(21):3873-82
pubmed: 17933793
Development. 2000 Feb;127(4):725-34
pubmed: 10648231
Dev Biol. 2004 Apr 15;268(2):506-13
pubmed: 15063185
Plant Cell. 2007 Apr;19(4):1278-94
pubmed: 17449808
Protoplasma. 2018 Jul;255(4):1053-1064
pubmed: 29404696
Development. 1996 Apr;122(4):1253-60
pubmed: 8620852
Genes Dev. 1994 Jun 15;8(12):1388-99
pubmed: 7926739
Plant Cell. 1999 Jul;11(7):1337-50
pubmed: 10402433
Proc Natl Acad Sci U S A. 2008 Jan 8;105(1):240-5
pubmed: 18172206
Curr Top Dev Biol. 2010;91:299-321
pubmed: 20705186
J Exp Bot. 2015 May;66(9):2515-26
pubmed: 25740926
Trends Plant Sci. 2000 May;5(5):214-9
pubmed: 10785667
PLoS One. 2016 Feb 04;11(2):e0148422
pubmed: 26845560
Plant Cell. 2013 Sep;25(9):3175-85
pubmed: 24014549
Plant Physiol. 1991 Jul;96(3):675-9
pubmed: 16668241
EMBO J. 2002 Oct 1;21(19):5036-46
pubmed: 12356720
Development. 2007 May;134(9):1691-701
pubmed: 17376813
Trends Plant Sci. 2006 Jun;11(6):274-80
pubmed: 16697247
Theor Appl Genet. 2016 Feb;129(2):305-16
pubmed: 26518574
Front Plant Sci. 2014 Jun 05;5:259
pubmed: 25018756
Nat Plants. 2016 Jun 20;2:16093
pubmed: 27322517
PLoS One. 2012;7(10):e47576
pubmed: 23110079
Plant Physiol. 2008 Nov;148(3):1583-602
pubmed: 18805951
Plant Cell. 1999 Jun;11(6):1105-16
pubmed: 10368181
Science. 1997 Aug 22;277(5329):1113-6
pubmed: 9262483
Ann Bot. 2013 May;111(5):821-37
pubmed: 23463590
Plant Cell. 1999 Jul;11(7):1217-26
pubmed: 10402424
Development. 1997 Oct;124(19):3779-86
pubmed: 9367433
New Phytol. 2009 Dec;184(4):988-1002
pubmed: 19761495
Genetics. 2000 Nov;156(3):1349-62
pubmed: 11063707
BMC Plant Biol. 2008 Jul 21;8:81
pubmed: 18644155
New Phytol. 2011 Jan;189(1):17-39
pubmed: 21054411
Biophys J. 2017 Nov 7;113(9):2068-2076
pubmed: 29117529
Development. 2002 Dec;129(23):5409-19
pubmed: 12403712
J Integr Plant Biol. 2012 Oct;54(10):729-37
pubmed: 22943441
Front Plant Sci. 2016 Aug 10;7:1187
pubmed: 27559338
Curr Opin Genet Dev. 2004 Aug;14(4):422-7
pubmed: 15261659
J Integr Plant Biol. 2015 Nov;57(11):925-35
pubmed: 25735194
Plant Mol Biol. 2016 Dec;92(6):675-687
pubmed: 27631431
Nat Rev Mol Cell Biol. 2004 Jun;5(6):471-80
pubmed: 15173826
BMC Plant Biol. 2015 Dec 29;15:302
pubmed: 26714637
Plant Cell. 1997 Jul;9(7):1109-20
pubmed: 9254933
Curr Opin Plant Biol. 2003 Feb;6(1):74-8
pubmed: 12495754
Plant J. 2002 Feb;29(3):359-69
pubmed: 11844112
J Exp Bot. 2007;58(6):1515-24
pubmed: 17347131
Philos Trans R Soc Lond B Biol Sci. 2000 Jul 29;355(1399):879-83
pubmed: 11128981
Philos Trans R Soc Lond B Biol Sci. 2002 Jun 29;357(1422):823-6
pubmed: 12079678
Plant Cell Environ. 2017 May;40(5):611-621
pubmed: 26920667
Plant J. 2011 Mar;65(5):785-97
pubmed: 21235650
Dev Biol. 2009 Jan 15;325(2):412-21
pubmed: 18992236
Development. 2008 Jun;135(11):1991-9
pubmed: 18434419
Plant J. 2004 Dec;40(6):860-9
pubmed: 15584952
New Phytol. 2015 Apr;206(1):10-13
pubmed: 25711246
Plant Mol Biol. 2004 May;55(3):389-98
pubmed: 15604688
Protoplasma. 2019 Nov;256(6):1531-1543
pubmed: 31190095