Rhytidome- and cork-type barks of holm oak, cork oak and their hybrids highlight processes leading to cork formation.
Cork
Cork oak
Holm oak
Hybrids
Outer bark
Periderm
Phellem
Rhytidome
Suberin
Journal
BMC plant biology
ISSN: 1471-2229
Titre abrégé: BMC Plant Biol
Pays: England
ID NLM: 100967807
Informations de publication
Date de publication:
03 Jun 2024
03 Jun 2024
Historique:
received:
02
08
2023
accepted:
23
05
2024
medline:
3
6
2024
pubmed:
3
6
2024
entrez:
2
6
2024
Statut:
epublish
Résumé
The periderm is basic for land plants due to its protective role during radial growth, which is achieved by the polymers deposited in the cell walls. In most trees, like holm oak, the first periderm is frequently replaced by subsequent internal periderms yielding a heterogeneous outer bark made of a mixture of periderms and phloem tissues, known as rhytidome. Exceptionally, cork oak forms a persistent or long-lived periderm which results in a homogeneous outer bark of thick phellem cell layers known as cork. Cork oak and holm oak distribution ranges overlap to a great extent, and they often share stands, where they can hybridize and produce offspring showing a rhytidome-type bark. Here we use the outer bark of cork oak, holm oak, and their natural hybrids to analyse the chemical composition, the anatomy and the transcriptome, and further understand the mechanisms underlying periderm development. We also include a unique natural hybrid individual corresponding to a backcross with cork oak that, interestingly, shows a cork-type bark. The inclusion of hybrid samples showing rhytidome-type and cork-type barks is valuable to approach cork and rhytidome development, allowing an accurate identification of candidate genes and processes. The present study underscores that abiotic stress and cell death are enhanced in rhytidome-type barks whereas lipid metabolism and cell cycle are enriched in cork-type barks. Development-related DEGs showing the highest expression, highlight cell division, cell expansion, and cell differentiation as key processes leading to cork or rhytidome-type barks. Transcriptome results, in agreement with anatomical and chemical analyses, show that rhytidome and cork-type barks are active in periderm development, and suberin and lignin deposition. Development and cell wall-related DEGs suggest that cell division and expansion are upregulated in cork-type barks whereas cell differentiation is enhanced in rhytidome-type barks.
Sections du résumé
BACKGROUND
BACKGROUND
The periderm is basic for land plants due to its protective role during radial growth, which is achieved by the polymers deposited in the cell walls. In most trees, like holm oak, the first periderm is frequently replaced by subsequent internal periderms yielding a heterogeneous outer bark made of a mixture of periderms and phloem tissues, known as rhytidome. Exceptionally, cork oak forms a persistent or long-lived periderm which results in a homogeneous outer bark of thick phellem cell layers known as cork. Cork oak and holm oak distribution ranges overlap to a great extent, and they often share stands, where they can hybridize and produce offspring showing a rhytidome-type bark.
RESULTS
RESULTS
Here we use the outer bark of cork oak, holm oak, and their natural hybrids to analyse the chemical composition, the anatomy and the transcriptome, and further understand the mechanisms underlying periderm development. We also include a unique natural hybrid individual corresponding to a backcross with cork oak that, interestingly, shows a cork-type bark. The inclusion of hybrid samples showing rhytidome-type and cork-type barks is valuable to approach cork and rhytidome development, allowing an accurate identification of candidate genes and processes. The present study underscores that abiotic stress and cell death are enhanced in rhytidome-type barks whereas lipid metabolism and cell cycle are enriched in cork-type barks. Development-related DEGs showing the highest expression, highlight cell division, cell expansion, and cell differentiation as key processes leading to cork or rhytidome-type barks.
CONCLUSION
CONCLUSIONS
Transcriptome results, in agreement with anatomical and chemical analyses, show that rhytidome and cork-type barks are active in periderm development, and suberin and lignin deposition. Development and cell wall-related DEGs suggest that cell division and expansion are upregulated in cork-type barks whereas cell differentiation is enhanced in rhytidome-type barks.
Identifiants
pubmed: 38825683
doi: 10.1186/s12870-024-05192-4
pii: 10.1186/s12870-024-05192-4
doi:
Substances chimiques
suberin
8072-95-5
Lipids
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
488Subventions
Organisme : Agencia Estatal de Investigación
ID : AGL2015-67495-C2-1-R (MINECO/FEDER,UE)
Organisme : Agencia Estatal de Investigación
ID : AGL2015-67495-C2-2-R (MINECO/FEDER,UE)
Organisme : Agencia Estatal de Investigación
ID : AGL2015-67495-C2-1-R (MINECO/FEDER,UE)
Organisme : Agencia Estatal de Investigación
ID : PID2019-110330GB-C21 (MCI/ AEI)
Organisme : Agencia Estatal de Investigación
ID : AGL2015-67495-C2-1-R (MINECO/FEDER,UE)
Organisme : Agencia Estatal de Investigación
ID : AGL2015-67495-C2-2-R (MINECO/FEDER,UE)
Organisme : Agencia Estatal de Investigación
ID : AGL2015-67495-C2-1-R (MINECO/FEDER,UE)
Organisme : Agencia Estatal de Investigación
ID : AGL2015-67495-C2-1-R (MINECO/FEDER,UE)
Organisme : Ministerio de Educación y Formación Profesional
ID : beca colaboración 2021_2022
Informations de copyright
© 2024. The Author(s).
Références
Serra O, Mähönen AP, Hetherington AJ, Ragni L. The making of Plant Armor: the Periderm. Annu Rev Plant Biol. 2022;73:405–32.
pubmed: 34985930
doi: 10.1146/annurev-arplant-102720-031405
Tonn N, Greb T. Radial plant growth. Curr Biol. 2017;27:R878–82.
pubmed: 28898657
doi: 10.1016/j.cub.2017.03.056
Howard ET. Bark structure of southern upland oaks. Wood Fiber Sci. 1977;9:172–83.
Evert RF, Esau K, Esau K. Esau’s plant anatomy: meristems, cells, and tissues of the plant body: their structure, function, and development. Hoboken, N.J.: Wiley-Interscience; 2006.
doi: 10.1002/0470047380
Romberger JA, Hejnowicz Z, Hill JF. Plant structure: function and development: a treatise on anatomy and vegetative development, with special reference to woody plants. Berlin; New York: Springer-; 1993.
Silva SP, Sabino MA, Fernandes EM, Correlo VM, Boesel LF, Reis RL. Cork: properties, capabilities and applications. Int Mater Rev. 2005;50:345–65.
doi: 10.1179/174328005X41168
Gil L. Cork: a strategic material. Front Chem. 2014;2:16.
pubmed: 24790984
pmcid: 3990040
doi: 10.3389/fchem.2014.00016
Boher P, Soler M, Sánchez A, Hoede C, Noirot C, Paiva JAP, et al. A comparative transcriptomic approach to understanding the formation of cork. Plant Mol Biol. 2018;96:103–18.
pubmed: 29143299
doi: 10.1007/s11103-017-0682-9
Meireles B, Usié A, Barbosa P, Fortes AM, Folgado A, Chaves I, et al. Characterization of the cork formation and production transcriptome in Quercus cerris × suber hybrids. Physiol Mol Biol Plants. 2018;24:535–49.
pubmed: 30042611
pmcid: 6041232
doi: 10.1007/s12298-018-0526-3
Burgarella C, Lorenzo Z, Jabbour-Zahab R, Lumaret R, Guichoux E, Petit RJ, et al. Detection of hybrids in nature: application to oaks (Quercus suber and Q. ilex). Heredity. 2009;102:442–52.
pubmed: 19240752
doi: 10.1038/hdy.2009.8
de Burgos G, Díez-Morales E, López de Heredia U, Soto Á. Qualitative and Quantitative Anatomical Analysis of the constitutive bark of Q. ilex x Q. Suber hybrids. Plants (Basel). 2022;11:2475.
pubmed: 36235341
doi: 10.3390/plants11192475
Ramos AM, Usié A, Barbosa P, Barros PM, Capote T, Chaves I, et al. The draft genome sequence of cork oak. Sci Data. 2018;5:180069.
pubmed: 29786699
pmcid: 5963338
doi: 10.1038/sdata.2018.69
de López U, Mora-Márquez F, Goicoechea PG, Guillardín-Calvo L, Simeone MC, Soto Á. ddRAD sequencing-based identification of genomic boundaries and permeability in Quercus ilex and Q. Suber hybrids. Front Plant Sci. 2020;11:564414.
pubmed: 33013984
pmcid: 7498617
doi: 10.3389/fpls.2020.564414
Conde E, García-Vallejo MC, Cadahía E. Waxes composition of Quercus suber reproduction cork from different Spanish provenances. Wood Sci Technol. 1999;33(4):271–83.
doi: 10.1007/s002260050115
Li Y, Beisson F, Koo AJK, Molina I, Pollard M, Ohlrogge J. Identification of acyltransferases required for cutin biosynthesis and production of cutin with suberin-like monomers. Proc Natl Acad Sci USA. 2007;104:18339–44.
pubmed: 17991776
pmcid: 2084344
doi: 10.1073/pnas.0706984104
Serra O, Soler M, Hohn C, Franke R, Schreiber L, Prat S, et al. Silencing of StKCS6 in potato periderm leads to reduced chain lengths of suberin and wax compounds and increased peridermal transpiration. J Exp Bot. 2009;60:697–07.
pubmed: 19112170
doi: 10.1093/jxb/ern314
Michaels SD, Bezerra IC, Amasino RM. FRIGIDA -related genes are required for the winter-annual habit in Arabidopsis. Proc Natl Acad Sci USA. 2004;101:3281–5.
pubmed: 14973192
pmcid: 365781
doi: 10.1073/pnas.0306778101
Schruff MC, Spielman M, Tiwari S, Adams S, Fenby N, Scott RJ. The AUXIN RESPONSE FACTOR 2 gene of Arabidopsis links auxin signalling, cell division, and the size of seeds and other organs. Development. 2006;133:251–61.
pubmed: 16339187
doi: 10.1242/dev.02194
Li SF, Milliken ON, Pham H, Seyit R, Napoli R, Preston J, et al. The Arabidopsis MYB5 transcription factor regulates mucilage synthesis, seed Coat Development, and Trichome Morphogenesis. Plant Cell. 2009;21:72–89.
pubmed: 19136646
pmcid: 2648076
doi: 10.1105/tpc.108.063503
Panikashvili D, Shi JX, Bocobza S, Franke RB, Schreiber L, Aharoni A. The Arabidopsis DSO/ABCG11 Transporter affects Cutin Metabolism in Reproductive organs and Suberin in roots. Mol Plant. 2010;3:563–75.
pubmed: 20035035
doi: 10.1093/mp/ssp103
Depuydt S, Rodriguez-Villalon A, Santuari L, Wyser-Rmili C, Ragni L, Hardtke CS. Suppression of Arabidopsis protophloem differentiation and root meristem growth by CLE45 requires the receptor-like kinase BAM3. Proc Natl Acad Sci USA. 2013;110:7074–9.
pubmed: 23569225
pmcid: 3637694
doi: 10.1073/pnas.1222314110
Haruta M, Sabat G, Stecker K, Minkoff BB, Sussman MR. A peptide hormone and its receptor protein kinase regulate plant cell expansion. Science. 2014;343:408–11.
pubmed: 24458638
pmcid: 4672726
doi: 10.1126/science.1244454
Liebsch D, Sunaryo W, Holmlund M, Norberg M, Zhang J, Hall HC, et al. Class I KNOX transcription factors promote differentiation of cambial derivatives into xylem fibers in the Arabidopsis hypocotyl. Development. 2014;141:4311–9.
pubmed: 25371365
doi: 10.1242/dev.111369
Bahieldin A, Atef A, Edris S, Gadalla NO, Ali HM, Hassan SM, et al. Ethylene responsive transcription factor ERF109 retards PCD and improves salt tolerance in plant. BMC Plant Biol. 2016;16:216.
pubmed: 27716054
pmcid: 5053207
doi: 10.1186/s12870-016-0908-z
Taylor I, Baer J, Calcutt R, Walker JC, Hypermorphic. SERK1 Mutations Function via a SOBIR1 Pathway to Activate Floral Abscission Signaling. Plant Physiol. 2019;180:1219–29.
Xiao W, Molina D, Wunderling A, Ripper D, Vermeer JEM, Ragni L. Pluripotent pericycle cells trigger different growth outputs by Integrating Developmental Cues into distinct Regulatory modules. Curr Biol. 2020;30:4384–e43985.
pubmed: 32916110
doi: 10.1016/j.cub.2020.08.053
Yordanov YS, Regan S, Busov V. Members of the LATERAL ORGAN BOUNDARIES DOMAIN transcription factor family are involved in the regulation of secondary growth in Populus. Plant Cell. 2010;22:3662–77.
pubmed: 21097711
pmcid: 3015109
doi: 10.1105/tpc.110.078634
Zhang J, Eswaran G, Alonso-Serra J, Kucukoglu M, Xiang J, Yang W, et al. Transcriptional regulatory framework for vascular cambium development in Arabidopsis roots. Nat Plants. 2019;5:1033–42.
pubmed: 31595065
pmcid: 6795544
doi: 10.1038/s41477-019-0522-9
Smit ME, McGregor SR, Sun H, Gough C, Bågman A-M, Soyars CL, et al. A PXY-Mediated Transcriptional Network integrates Signaling mechanisms to control Vascular Development in Arabidopsis. Plant Cell. 2020;32:319–35.
pubmed: 31806676
doi: 10.1105/tpc.19.00562
Almeida T, Pinto G, Correia B, Santos C, Gonçalves S. QsMYB1 expression is modulated in response to heat and drought stresses and during plant recovery in Quercus suber. Plant Physiol Biochem. 2013;73:274–81.
pubmed: 24161757
doi: 10.1016/j.plaphy.2013.10.007
Miguel A, Milhinhos A, Novák O, Jones B, Miguel CM. The SHORT-ROOT -like gene PtSHR2B is involved in Populus phellogen activity. J Exp Bot. 2016;67:1545–55.
pubmed: 26709311
doi: 10.1093/jxb/erv547
Capote T, Barbosa P, Usié A, Ramos AM, Inácio V, Ordás R, et al. ChIP-Seq reveals that QsMYB1 directly targets genes involved in lignin and suberin biosynthesis pathways in cork oak (Quercus suber). BMC Plant Biol. 2018;18:198.
pubmed: 30223777
pmcid: 6142680
doi: 10.1186/s12870-018-1403-5
Wang C, Wang H, Li P, Li H, Xu C, Cohen H, et al. Developmental programs interact with abscisic acid to coordinate root suberization in Arabidopsis. Plant J. 2020;104:241–51.
pubmed: 32645747
doi: 10.1111/tpj.14920
Rojas-Murcia N, Hématy K, Lee Y, Emonet A, Ursache R, Fujita S, et al. High-order mutants reveal an essential requirement for peroxidases but not laccases in Casparian strip lignification. Proc Natl Acad Sci USA. 2020;117:29166–77.
pubmed: 33139576
pmcid: 7682338
doi: 10.1073/pnas.2012728117
Krishnamurthy P, Vishal B, Ho WJ, Lok FCJ, Lee FSM, Kumar PP. Regulation of a cytochrome P450 gene CYP94B1 by WRKY33 transcription factor controls apoplastic barrier formation in roots to Confer Salt Tolerance. Plant Physiol. 2020;184:2199–215.
pubmed: 32928900
pmcid: 7723105
doi: 10.1104/pp.20.01054
Krishnamurthy P, Vishal B, Bhal A, Kumar PP. WRKY9 transcription factor regulates cytochrome P450 genes CYP94B3 and CYP86B1, leading to increased root suberin and salt tolerance in Arabidopsis. Physiol Plant. 2021;172:1673–87.
pubmed: 33619745
doi: 10.1111/ppl.13371
Andersen TG, Molina D, Kilian J, Franke RB, Ragni L, Geldner N. Tissue-Autonomous Phenylpropanoid production is essential for establishment of Root barriers. Curr Biol. 2021;31:965–e9775.
pubmed: 33529644
doi: 10.1016/j.cub.2020.11.070
Mishra G, Zhang W, Deng F, Zhao J, Wang X. A bifurcating pathway directs Abscisic Acid effects on Stomatal Closure and opening in Arabidopsis. Science. 2006;312:264–6.
pubmed: 16614222
doi: 10.1126/science.1123769
Drakakaki G, Zabotina O, Delgado I, Robert S, Keegstra K, Raikhel N. Arabidopsis Reversibly Glycosylated polypeptides 1 and 2 are essential for Pollen Development. Plant Physiol. 2006;142:1480–92.
pubmed: 17071651
pmcid: 1676068
doi: 10.1104/pp.106.086363
Cannon MC, Terneus K, Hall Q, Tan L, Wang Y, Wegenhart BL, et al. Self-assembly of the plant cell wall requires an extensin scaffold. Proc Natl Acad Sci USA. 2008;105:2226–31.
pubmed: 18256186
pmcid: 2538902
doi: 10.1073/pnas.0711980105
Kurasawa K, Matsui A, Yokoyama R, Kuriyama T, Yoshizumi T, Matsui M, et al. The AtXTH28 gene, a Xyloglucan Endotransglucosylase/Hydrolase, is involved in Automatic Self-Pollination in Arabidopsis thaliana. Plant Cell Physiol. 2008;50:413–22.
doi: 10.1093/pcp/pcp003
Guo H, Li L, Ye H, Yu X, Algreen A, Yin Y. Three related receptor-like kinases are required for optimal cell elongation in Arabidopsis thaliana. Proc Natl Acad Sci U S A. 2009;106:7648–53.
pubmed: 19383785
pmcid: 2678668
doi: 10.1073/pnas.0812346106
Takahashi J, Rudsander UJ, Hedenström M, Banasiak A, Harholt J, Amelot N, et al. KORRIGAN1 and its Aspen Homolog PttCel9A1 decrease cellulose crystallinity in Arabidopsis stems. Plant Cell Physiol. 2009;50:1099–115.
pubmed: 19398462
doi: 10.1093/pcp/pcp062
Compagnon V, Diehl P, Benveniste I, Meyer D, Schaller H, Schreiber L, et al. CYP86B1 is required for very long chain omega-hydroxyacid and alpha, omega -dicarboxylic acid synthesis in root and seed suberin polyester. Plant Physiol. 2009;150:1831–43.
pubmed: 19525321
pmcid: 2719127
doi: 10.1104/pp.109.141408
Gou J-Y, Yu X-H, Liu C-J. A hydroxycinnamoyltransferase responsible for synthesizing suberin aromatics in Arabidopsis. Proc Natl Acad Sci U S A. 2009;106:18855–60.
pubmed: 19846769
pmcid: 2773987
doi: 10.1073/pnas.0905555106
Molina I, Li-Beisson Y, Beisson F, Ohlrogge JB, Pollard M. Identification of an Arabidopsis Feruloyl-Coenzyme A Transferase required for suberin synthesis. Plant Physiol. 2009;151:1317–28.
pubmed: 19759341
pmcid: 2773081
doi: 10.1104/pp.109.144907
Krupková E, Schmülling T. Developmental consequences of the tumorous shoot development1 mutation, a novel allele of the cellulose-synthesizing KORRIGAN1 gene. Plant Mol Biol. 2009;71:641–55.
pubmed: 19826767
doi: 10.1007/s11103-009-9546-2
Serra O, Hohn C, Franke R, Prat S, Molinas M, Figueras M. A feruloyl transferase involved in the biosynthesis of suberin and suberin-associated wax is required for maturation and sealing properties of potato periderm: FHT function in potato periderm. Plant J. 2010;62:277–90.
pubmed: 20088895
doi: 10.1111/j.1365-313X.2010.04144.x
Reboul R, Geserick C, Pabst M, Frey B, Wittmann D, Lütz-Meindl U, et al. Down-regulation of UDP-glucuronic Acid Biosynthesis leads to Swollen Plant cell walls and severe Developmental defects Associated with changes in Pectic Polysaccharides. J Biol Chem. 2011;286:39982–92.
pubmed: 21949134
pmcid: 3220558
doi: 10.1074/jbc.M111.255695
Jin H, Song Z, Nikolau BJ. Reverse genetic characterization of two paralogous acetoacetyl CoA thiolase genes in Arabidopsis reveals their importance in plant growth and development. Plant J. 2012;70:1015–32.
pubmed: 22332816
doi: 10.1111/j.1365-313X.2012.04942.x
Chen Y, Zou T, McCormick S. -Adenosylmethionine synthetase 3 is important for Pollen Tube Growth. Plant Physiol. 2016;172:244–53.
pubmed: 27482079
pmcid: 5074607
doi: 10.1104/pp.16.00774
Deeken R, Saupe S, Klinkenberg J, Riedel M, Leide J, Hedrich R, et al. The nonspecific lipid transfer protein AtLtpI-4 is involved in suberin formation of Arabidopsis thaliana Crown Galls. Plant Physiol. 2016;172:1911–27.
pubmed: 27688623
pmcid: 5100791
doi: 10.1104/pp.16.01486
Smetana O, Mäkilä R, Lyu M, Amiryousefi A, Sánchez Rodríguez F, Wu M-F, et al. High levels of auxin signalling define the stem-cell organizer of the vascular cambium. Nature. 2019;565:485–9.
pubmed: 30626967
doi: 10.1038/s41586-018-0837-0
Beisson F, Li Y, Bonaventure G, Pollard M, Ohlrogge JB. The acyltransferase GPAT5 is required for the synthesis of suberin in seed coat and root of Arabidopsis. Plant Cell. 2007;19:351–68.
pubmed: 17259262
pmcid: 1820950
doi: 10.1105/tpc.106.048033
Franke R, Höfer R, Briesen I, Emsermann M, Efremova N, Yephremov A, et al. The DAISY gene from Arabidopsis encodes a fatty acid elongase condensing enzyme involved in the biosynthesis of aliphatic suberin in roots and the chalaza-micropyle region of seeds. Plant J. 2009;57:80–95.
pubmed: 18786002
doi: 10.1111/j.1365-313X.2008.03674.x
Lee S-B, Jung S-J, Go Y-S, Kim H-U, Kim J-K, Cho H-J, et al. Two Arabidopsis 3-ketoacyl CoA synthase genes, KCS20 and KCS2/DAISY, are functionally redundant in cuticular wax and root suberin biosynthesis, but differentially controlled by osmotic stress. Plant J. 2009;60:462–75.
pubmed: 19619160
doi: 10.1111/j.1365-313X.2009.03973.x
Domergue F, Vishwanath SJ, Joubès J, Ono J, Lee JA, Bourdon M, et al. Three Arabidopsis fatty acyl-coenzyme A reductases, FAR1, FAR4, and FAR5, Generate Primary Fatty Alcohols Associated with Suberin Deposition. Plant Physiol. 2010;153:1539–54.
pubmed: 20571114
pmcid: 2923872
doi: 10.1104/pp.110.158238
Yadav V, Molina I, Ranathunge K, Castillo IQ, Rothstein SJ, Reed JW. ABCG transporters are required for suberin and Pollen Wall Extracellular barriers in Arabidopsis. Plant Cell. 2014;26:3569–88.
pubmed: 25217507
pmcid: 4213157
doi: 10.1105/tpc.114.129049
Ursache R, De Jesus Vieira Teixeira C, Dénervaud Tendon V, Gully K, De Bellis D, Schmid-Siegert E, et al. GDSL-domain proteins have key roles in suberin polymerization and degradation. Nat Plants. 2021;7:353–64.
pubmed: 33686223
pmcid: 7610369
doi: 10.1038/s41477-021-00862-9
Kamiya T, Borghi M, Wang P, Danku JMC, Kalmbach L, Hosmani PS, et al. The MYB36 transcription factor orchestrates casparian strip formation. Proc Natl Acad Sci USA. 2015;112:10533–8.
pubmed: 26124109
pmcid: 4547244
doi: 10.1073/pnas.1507691112
Lashbrooke J, Cohen H, Levy-Samocha D, Tzfadia O, Panizel I, Zeisler V, et al. MYB107 and MYB9 homologs regulate suberin deposition in Angiosperms. Plant Cell. 2016;28:2097–116.
pubmed: 27604696
pmcid: 5059810
doi: 10.1105/tpc.16.00490
Legay S, Guerriero G, André C, Guignard C, Cocco E, Charton S, et al. MdMyb93 is a regulator of suberin deposition in russeted apple fruit skins. New Phytol. 2016;212:977–91.
pubmed: 27716944
doi: 10.1111/nph.14170
Wei X, Mao L, Wei X, Xia M, Xu C. MYB41, MYB107, and MYC2 promote ABA-mediated primary fatty alcohol accumulation via activation of AchnFAR in wound suberization in kiwifruit. Hortic Res. 2020;7:86.
pubmed: 32528698
pmcid: 7261769
doi: 10.1038/s41438-020-0309-1
Wahrenburg Z, Benesch E, Lowe C, Jimenez J, Vulavala VKR, Lü S, et al. Transcriptional regulation of wound suberin deposition in potato cultivars with differential wound healing capacity. Plant J. 2021;107:77–99.
pubmed: 33860574
doi: 10.1111/tpj.15275
Verdaguer R, Soler M, Serra O, Garrote A, Fernández S, Company-Arumí D, et al. Silencing of the potato StNAC103 gene enhances the accumulation of suberin polyester and associated wax in tuber skin. J Exp Bot. 2016;67:5415–27.
pubmed: 27520790
pmcid: 5049391
doi: 10.1093/jxb/erw305
Mudunkothge JS, Krizek BA. Three Arabidopsis AIL/PLT genes act in combination to regulate shoot apical meristem function: AIL/PLT genes regulate meristem function. Plant J. 2012;71:108–21.
pubmed: 22380923
doi: 10.1111/j.1365-313X.2012.04975.x
Alonso-Serra J, Safronov O, Lim K, Fraser‐Miller SJ, Blokhina OB, Campilho A, et al. Tissue‐specific study across the stem reveals the chemistry and transcriptome dynamics of birch bark. New Phytol. 2019;222:1816–31.
pubmed: 30724367
doi: 10.1111/nph.15725
Holloway PJ. Some variations in the composition of suberin from the cork layers of higher plants. Phytochemistry. 1983;22:495–502.
doi: 10.1016/0031-9422(83)83033-7
Jin H, Hu W, Wei Z, Wan L, Li G, Tan G, Zhu L, He G. Alterations in cytosine methylation and species-specific transcription induced by interspecific hybridization between Oryza sativa and O. Officinalis. Theor Appl Genet. 2008;117:1271–79.
pubmed: 18719877
doi: 10.1007/s00122-008-0861-9
Czypionka T, Cheng J, Pozhitkov A, Nolte AW. Transcriptome changes after genome-wide admixture in invasive sculpins (Cottus). Mol Ecol. 2012;21:4797–810.
pubmed: 22650446
doi: 10.1111/j.1365-294X.2012.05645.x
Liang S, Luo X, You W, Ke C. Hybridization improved bacteria resistance in abalone: evidence from physiological and molecular responses. Fish Shellfish Immun. 2018;72:679–89.
doi: 10.1016/j.fsi.2017.11.009
Silvert M, Quintana-Murci L, Rotival M. Impact and evolutionary determinants of Ne-anderthal introgression on transcriptional and post-transcriptional regulation. Am J Hum Genet. 2019;104:1241–50.
pubmed: 31155285
pmcid: 6557732
doi: 10.1016/j.ajhg.2019.04.016
Kong X, Chen L, Wei T, Zhou H, Bai C, Yan X, Miao Z, Xie J, Zhang L. Transcriptome analysis of biological pathways associated with heterosis in Chinese cabbage. Genome., Duan Q, Liu M-CJ, Kita D, Jordan SS, Yeh F-LJ, Yvon R et al. FERONIA controls pectin- and nitric oxide-mediated male–female interaction. Nature. 2020;579:561–6.
Tabata R, Ikezaki M, Fujibe T, Aida M, Tian C, Ueno Y, et al. Arabidopsis AUXIN RESPONSE FACTOR6 and 8 regulate Jasmonic Acid Biosynthesis and Floral Organ Development via repression of class 1 KNOX genes. Plant Cell Physiol. 2010;51:164–75.
pubmed: 20007966
doi: 10.1093/pcp/pcp176
Paredez AR, Persson S, Ehrhardt DW, Somerville CR. Genetic evidence that cellulose synthase activity influences Microtubule cortical array Organization. Plant Physiol. 2008;147:1723–34.
pubmed: 18583534
pmcid: 2492609
doi: 10.1104/pp.108.120196
Yan J, Huang Y, He H, Han T, Di P, Sechet J, et al. Xyloglucan endotransglucosylase-hydrolase30 negatively affects salt tolerance in Arabidopsis. J Exp Bot. 2019;70:5495–506.
pubmed: 31257449
pmcid: 6793456
doi: 10.1093/jxb/erz311
Daher FB, Braybrook SA. How to let go: pectin and plant cell adhesion. Front Plant Sci. 2015;6:523.
pubmed: 26236321
pmcid: 4500915
doi: 10.3389/fpls.2015.00523
Patharkar OR, Walker JC. Advances in abscission signaling. J Exp Bot. 2018;69:733–40.
pubmed: 28992277
doi: 10.1093/jxb/erx256
Lee Y, Yoon TH, Lee J, Jeon SY, Lee JH, Lee MK, et al. A lignin Molecular Brace Controls Precision Processing of cell walls critical for Surface Integrity in Arabidopsis. Cell. 2018;173:1468–e14809.
pubmed: 29731167
doi: 10.1016/j.cell.2018.03.060
Jové P, Olivella À, Cano L. Study of the variability in chemical composition of bark layers of Quercus suber L. from different production areas. BioResources. 2011;6:1806–15.
doi: 10.15376/biores.6.2.1806-1815
Wise LE, Ratliff EK. (1947). Quantitative isolation of hemicelluloses and summative analysis of wood. Anal Chem. 1947;19(7):459–462.
Chang S, Puryear J, Cairney J. A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Rep. 1993;11:113–6.
doi: 10.1007/BF02670468
Chaves I, Lin Y-C, Pinto-Ricardo C, Van de Peer Y, Miguel C. miRNA profiling in leaf and cork tissues of Quercus suber reveals novel miRNAs and tissue-specific expression patterns. Tree Genet Genomes. 2014;10:721–37.
doi: 10.1007/s11295-014-0717-1
Andrews S. FastQC: a quality control tool for high throughput sequence data. Cambridge, United Kingdom: Babraham Bioinformatics, Babraham Institute; 2010.
Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–20.
pubmed: 24695404
pmcid: 4103590
doi: 10.1093/bioinformatics/btu170
Wu TD, Reeder J, Lawrence M, Becker G, Brauer MJ. GMAP and GSNAP for genomic sequence alignment: Enhancements to Speed, Accuracy, and functionality. Methods Mol Biol. 2016;1418:283–334.
pubmed: 27008021
doi: 10.1007/978-1-4939-3578-9_15
Anders S, Pyl PT, Huber W. HTSeq–a Python framework to work with high-throughput sequencing data. Bioinformatics. 2015;31:166–9.
pubmed: 25260700
doi: 10.1093/bioinformatics/btu638
Love MI, Huber W, Anders S. Moderated estimation of Fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:550.
pubmed: 25516281
pmcid: 4302049
doi: 10.1186/s13059-014-0550-8
Wickham H. ggplot2. Elegant Graphics for Data Analysis. New York, NY: Springer; 2009.
doi: 10.1007/978-0-387-98141-3
Howe E, Holton K, Nair S, Schlauch D, Sinha R, Quackenbush J. MeV: MultiExperiment Viewer. In: Ochs MF, Casagrande JT, Davuluri RV, editors. Biomedical Informatics for Cancer Research. Boston, MA: Springer US; 2010. pp. 267–77.
doi: 10.1007/978-1-4419-5714-6_15
Tian T, Liu Y, Yan H, You Q, Yi X, Du Z, et al. agriGO v2.0: a GO analysis toolkit for the agricultural community, 2017 update. Nucleic Acids Res. 2017;45:W122–9.
pubmed: 28472432
pmcid: 5793732
doi: 10.1093/nar/gkx382
Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001;29:e45–45.
pubmed: 11328886
pmcid: 55695
doi: 10.1093/nar/29.9.e45
Soler M, Serra O, Molinas M, Garcia-Berthou E, Caritat A, Figueras M. Seasonal variation in transcript abundance in cork tissue analyzed by real time RT-PCR. Tree Physiol. 2008;28:743–51.
pubmed: 18316306
doi: 10.1093/treephys/28.5.743
Junikka L. Survey of English macroscopic bark terminology. IAWA J. 1994;15:3–45.
doi: 10.1163/22941932-90001338