Abstract
Secondary or lateral growth, is the biological process that confers girth to stems and roots in plants, which is essential to structurally sustain organs, for water and nutrients transport and continuous plant growth. This process occurs at the expense of the cell division activity in two main lateral meristems—the vascular cambium and the cork cambium. From the activity of cambia, one of the main sources of biomass on Earth, wood, is produced. Given its economic, environmental and societal relevance a great deal of attention has been given to finding regulators of vascular cambium activity and wood formation. Some of the regulatory networks found are under post-transcriptional regulation of gene expression by microRNAs during vasculature formation, cambium activity, and wood formation and in several aspects of vascular development. In this chapter, we will briefly review the current knowledge on microRNAs roles during plant vascular development with a focus on recent work on miRNAs activity in secondary growth in plants.
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References
Almeida T, Menendez E, Capote T et al (2013a) Molecular characterization of Quercus suber MYB1, a transcription factor up-regulated in cork tissues. J Plant Physiol 170:172–178
Almeida T, Pinto G, Correia B et al (2013b) QsMYB1 expression is modulated in response to heat and drought stresses and during plant recovery in Quercus suber. Plant Physiol Biochem 73:274–281
Alonso-Serra J, Safronov O, Lim K et al (2019) Tissue-specific study across the stem reveals the chemistry and transcriptome dynamics of birch bark. New Phytol 222:1816–1831
Aukerman MJ, Sakai H (2003) Regulation of flowering time and floral organ identity by a MicroRNA and its APETALA2-like target genes. Plant Cell 15:2730–2741
Baima S, Nobili F, Sessa G et al (1995) The expression of the ATHB-8 homeobox gene is restricted to provascular cells in Arabidopsis thaliana. Development 121:4171–4182
Baima S, Possenti M, Matteucci A et al (2001) The Arabidopsis ATHB-8 HD-ZIP protein acts as a differentiation-promoting transcription factor of the vascular meristems. Plant Physiol 126:643–655
Barakat A, Wall PK, Diloreto S et al (2007) Conservation and divergence of microRNAs in Populus. BMC Genom 8:481
Bartel B, Bartel DP (2003) MicroRNAs: at the root of plant development? Plant Physiol 132:709–717
Benfey PN, Linstead PJ, Roberts K et al (1993) Root development in Arabidopsis: four mutants with dramatically altered root morphogenesis. Development 119:57–70
Boher P, Soler M, Sánchez A et al (2018) A comparative transcriptomic approach to understanding the formation of cork. Plant Mol Biol 96:103–118
Bossinger G, Spokevicius AV (2018) Sector analysis reveals patterns of cambium differentiation in poplar tree stems. J Exp Bot 69:4339–4348
Campilho A, Nieminen K, Ragni L (2020) The development of the periderm: the final frontier between a plant and its environment. Curr Opin Plant Biol 53:10–14
Capote T, Barbosa P, Usié A et al (2018) ChIP-Seq reveals that QsMYB1 directly targets genes involved in lignin and suberin biosynthesis pathways in cork oak (Quercus suber). BMC Plant Biol 18:198
Carlsbecker A, Lee JY, Roberts CJ et al (2010) Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate. Nature 465:316–321
Chaves I, Lin Y-C, Pinto-Ricardo C et al (2014) miRNA profiling in leaf and cork tissues of Quercus suber reveals novel miRNAs and tissue-specific expression patterns. Tree Genet Genomes 10:721–737
Chen J, Chen B, Yang X et al (2015a) Association genetics in Populus reveals the interactions between Pt-miR397a and its target genes. Sci Rep 5:11672
Chen J, Quan M, Zhang D (2015b) Genome-wide identification of novel long non-coding RNAs in Populus tomentosa tension wood, opposite wood and normal wood xylem by RNA-seq. Planta 241:125
Chen B, Du Q, Chen J et al (2016a) Dissection of allelic interactions among Pto-miR257 and its targets and their effects on growth and wood properties in Populus. Heredity 117:73–83
Chen J, Xie J, Chen B et al (2016b) Genetic variations and miRNA–target interactions contribute to natural phenotypic variations in Populus. New Phytol 212:150–160
Couzigou JM, Combier JP (2016) Plant microRNAs: key regulators of root architecture and biotic interactions. New Phytol 212:22–35
Cui J, Lu W, Lu Z et al (2019) Identification and analysis of microRNAs in the SAM and leaves of Populus tomentosa. Forests 10:130
Dastidar MG, Mosiolek M, Bleckmann A et al (2016) Sensitive whole mount in situ localization of small RNAs in plants. Plant J 88:694–702
Digby J, Wareing PF (1966) The effect of applied growth hormones on cambial division and the differentiation of the cambial derivatives. Ann Bot 30:539–548
Ding Q, Zeng J, He XQ (2014) Deep sequencing on a genome-wide scale reveals diverse stage-specific microRNAs in cambium during dormancy-release induced by chilling in poplar. BMC Plant Biol 14:267
Dolan L, Janmaat K, Willemsen V (1993) Cellular organisation of the Arabidopsis thaliana root. Development 119:71–84
Du J, Miura E, Robischon M et al (2011) The Populus Class III HD ZIP Transcription Factor POPCORONA Affects Cell Differentiation during Secondary Growth of Woody Stems. PLoS ONE 6:e17458
Du Q, Avci U, Li S et al (2015) Activation of miR165b represses AtHB15 expression and induces pith secondary wall development in Arabidopsis. Plant J 83:388–400
Ebert MS, Sharp PA (2010) Emerging roles for natural microRNA sponges. Curr Biol 20:R858–R861
Emery JF, Floyd SK, Alvarez J et al (2003) Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes. Curr Biol 13:1768–1774
Esau K (ed) (1960) Anatomy of seed plants. Wiley, New York, p 376
Evans LM, Slavov GT, Rodgers-Melnick R et al (2014) Population genomics of Populus trichocarpa identifies signatures of selection and adaptive trait associations. Nat Genet 46:1089–1096
Felipo-Benavent A, Úrbez C, Blanco-Touriñán N et al (2018) Regulation of xylem fiber differentiation by gibberellins through DELLA-KNAT1 interaction. Development 145:dev164962
Graça J, Pereira H (2004) The periderm development in Quercus suber. IAWA J 25:325–335
Guo C, Xu Y, Shi M et al (2017) Repression of miR156 by miR159 regulates the timing of the juvenile-to-adult transition in Arabidopsis. Plant Cell 29:1293–1304
He F, Xu C, Fu X et al (2018) The MicroRNA390/TRANS-ACTING SHORT INTERFERING RNA3 module mediates lateral root growth under salt stress via the auxin pathway. Plant Physiol 177:775–791
Hirakawa Y, Kondo Y, Fukuda H (2010) TDIF peptide signaling regulates vascular stem cell proliferation via the WOX4 homeobox gene in Arabidopsis. Plant Cell 22:2618–2629
Huijser P, Schmid M (2011) The control of developmental phase transitions in plants. Development 138:4117–4129
Ilegems M, Douet V, Meylan-Bettex M et al (2010) Interplay of auxin, KANADI and Class III HD-ZIP transcription factors in vascular tissue formation. Development 137:975–984
Inácio V, Martins MT, Graça J et al (2018) Cork oak young and traumatic periderms show PCD typical chromatin patterns but different chromatin-modifying genes expression. Front Plant Sci 9
Izhaki A, Bowman JL (2007) KANADI and class III HD-Zip gene families regulate embryo patterning and modulate auxin flow during embryogenesis in Arabidopsis. Plant Cell 19:495–508
Ji L, Liu X, Yan J et al (2011) ARGONAUTE10 and ARGONAUTE1 regulate the termination of floral stem cells through two microRNAs in Arabidopsis. PLoS Genet 7:e1001358
Kerstetter RA, Bollman K, Taylor RA et al (2001) KANADI regulates organ polarity in Arabidopsis. Nature 411:706–709
Kim J, Jung J-H, Reyes JL et al (2005) microRNA-directed cleavage of ATHB15 mRNA regulates vascular development in Arabidopsis inflorescence stems. Plant J 42:84–94
Klevebring D, Street NR, Fahlgren N et al (2009) Genome-wide profiling of Populus small RNAs. BMC Genom 10:620
Ko J-H, Prassinos C, Han K-H (2006) Developmental and seasonal expression of PtaHB1, a Populus gene encoding a class III HD-Zip protein, is closely associated with secondary growth and inversely correlated with the level of microRNA (miR166). New Phytol 169:469–478
Kozomara A, Griffiths-Jones S (2014) miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res 42(Database issue):D68–D73
Le Roy J, Blervacq AS, Créach A et al (2017) Spatial regulation of monolignol biosynthesis and laccase genes control developmental and stress-related lignin in flax. BMC Plant Biol 17:124
Li C, Lu S (2014) Molecular characterization of the SPL gene family in Populus trichocarpa. BMC Plant Biol 14:131
Liebsch D, Sunaryo W, Holmlund M et al (2014) Class I KNOX transcription factors promote differentiation of cambial derivatives into xylem fibers in the Arabidopsis hypocotyl. Development 141:4311–4319
Lu S, Sun Y-H, Shi R et al (2005) Novel and mechanical stress-responsive microRNAs in Populus trichocarpa that are absent from Arabidopsis. Plant Cell 17:2186–2203
Lu S, Li Q, Wei H et al (2013) Ptr-miR397a is a negative regulator of laccase genes affecting lignin content in Populus trichocarpa. Proc Natl Acad Sci USA 110:10848–10853
Mallory AC, Bartel DP, Bartel B (2005) MicroRNA-directed regulation of Arabidopsis AUXIN RESPONSE FACTOR17 is essential for proper development and modulates expression of early auxin response genes. Plant Cell 17:1360–1375
Mallory AC, Reinhart BJ, Jones-Rhoades MW et al (2004) MicroRNA control of PHABULOSA in leaf development: importance of pairing to the microRNA 5′ region. EMBO J 23:3356–3364
Marin-Gonzalez E, Suarez-Lopez P (2012) “And yet it moves”: cell-to-cell and long-distance signaling by plant microRNAs. Plant Sci 196:18–30
Mauriat M, Moritz T (2009) Analyses of GA20ox- and GID1-over-expressing aspen suggest that gibberellins play two distinct roles in wood formation. Plant J 58:989–1003
McConnell JR, Barton MK (1998) Leaf polarity and meristem formation in Arabidopsis. Development 125:2935–2942
McConnell JR, Emery J, Eshed Y et al (2001) Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature 411:709–713
Miguel A, Milhinhos A, Novak et al (2016) The SHORT‐ROOT‐like gene PtSHR2B is involved in Populus phellogen activity. J Exp Bot 67:1545–1555
Milhinhos A, Prestele J, Bollhoner B et al (2013) Thermospermine levels are controlled by an auxin-dependent feedback loop mechanism in Populus xylem. Plant J 75:685–698
Milhinhos A, Vera-Sirera F, Blanco-Touriñán N et al (2019) SOBIR1/EVR prevents precocious initiation of fiber differentiation during wood development through a mechanism involving BP and ERECTA. Proc Natl Acad Sci USA 116:18710–18716
Miyashima S, Koi S, Hashimoto T (2011) Non-cell-autonomous microRNA165 acts in a dose-dependent manner to regulate multiple differentiation status in the Arabidopsis root. Development 138:2303–2313
Miyashima S, Roszak P, Sevilem I et al (2019) Mobile PEAR transcription factors integrate hormone and miRNA cues to prime cambial growth. Nature 565:490–494
Natividade JV (ed) (1950) Subericultura. DGSFA, Lisboa
Ohashi-Ito K, Fukuda H (2003) HD-Zip III homeobox genes that include a novel member, ZeHB-13 (Zinnia)/ATHB-15 (Arabidopsis), are involved in procambium and xylem cell differentiation. Plant Cell Physiol 44:1350–1358
Otsuga D, DeGuzman B, Prigge MJ et al (2001) REVOLUTA regulates meristem initiation at lateral positions. Plant J. 25:223–236
Pereira-Leal JB, Abreu IA, Alabaça CS et al (2014) A comprehensive assessment of the transcriptome of cork oak (Quercus suber) through EST sequencing. BMC Genom 15:371
Porth I, Klápste J, McKown AD et al (2014) Extensive functional pleiotropy of REVOLUTA substantiated through forward genetics. Plant Physiol 164:548–554
Potkar R, Recla J, Busov V (2013) ptr-MIR169 is a posttranscriptional repressor of PtrHAP2 during vegetative bud dormancy period of aspen (Populus tremuloides) trees. Biochem Biophys Res Commun 431:512–518
Prigge MJ, Otsuga D, Alonso JM et al (2005) Class III homeodomain-leucine zipper gene family members have overlapping, antagonistic, and distinct roles in Arabidopsis development. Plant Cell 17:61–76
Puzey JR, Karger A, Axtell M et al (2012) Deep annotation of Populus trichocarpa microRNAs from diverse tissue sets. PLoS ONE 7:e33034
Qiu Z, Li X, Zhao Y et al (2015) Genome-wide analysis reveals dynamic changes in expression of microRNAs during vascular cambium development in Chinese fir, Cunninghamia lanceolata. J Exp Bot 66:3041–3054
Quan M, Wang Q, Phangthavong S et al (2016) Association studies in Populus tomentosa reveal the genetic interactions of Pto-MIR156c and its targets in wood formation. Front Plant Sci 7:1159
Quan M, Xiao L, Lu W et al (2018) Association genetics in Populus reveal the allelic interactions of Pto-MIR167a and its targets in wood formation. Front Plant Sci 9:744
Quan M, Du Q, Xiao L et al (2019) Genetic architecture underlying the lignin biosynthesis pathway involves noncoding RNAs and transcription factors for growth and wood properties in Populus. Plant Biotechnol J 17:302–315
Ragni L, Nieminen K, Pacheco-Villalobos D et al (2011) Mobile gibberellin directly stimulates arabidopsis hypocotyl xylem expansion. Plant Cell 23:1322–1336
Ramachandran P, Carlsbecker A, Etchells P (2017) Class III HD-ZIPs govern vascular cell fate: an HD view on patterning and differentiation. J Exp Bot 68:55–69
Ramos AM, Usié A, Barbosa P et al (2018) The draft genome sequence of cork oak. Sci Data 5:180069
Randall RS, Miyashima S, Blomster T et al (2015) AINTEGUMENTA and the D type cyclin CYCD3;1 regulate root secondary growth and respond to cytokinins. Biol Open 4:1229–1236
Ratcliffe OJ, Riechmann JL, Zhang JZ (2000) INTERFASCICULAR FIBERLESS1 is the same gene as REVOLUTA. Plant Cell 12:315–317
Reinhart BJ, Weinstein EG, Rhoades MW et al (2002) MicroRNAs in plants. Genes Dev 16:1616–1626
Rhoades MW, Reinhart BJ, Lim LP et al (2002) Prediction of plant microRNA targets. Cell 110:513–520
Ridoutt BG, Pharis RP, Sands R (1996) Fibre length and gibberellins A1 and A20 are decreased in Eucalyptus globulus by acylcyclohexanedione injected into stem. Physiol Plant 96:559–566
Robischon M, Du J, Miura E, Groover A (2011) The Populus class III HD ZIP, popREVOLUTA, influences cambium initiation and patterning of woody stems. Plant Physiol 155(3):1214–1225. https://doi.org/10.1104/pp.110.167007
Rodriguez RE, Ercoli MF, Debernardi JM et al (2015) MicroRNA miR396 regulates the switch between stem cells and transit-amplifying cells in Arabidopsis roots. Plant Cell 27:3354–3366
Sakaguchi J, Watanabe Y (2012) miR165/166 and the development of land plants. Dev Growth Differ 54:93–99
Scheres B, Wolkenfelt H, Willemsen V et al (1994) Embryonic origin of the Arabidopsis primary root and root meristem initials. Development 120:2475–2487
Shi W, Quan M, Du Q et al (2017) The interactions between the long non-coding RNA NERDL and its target gene affect wood formation in Populus tomentosa. Front Plant Sci 8:1035
Shi D, Lebovka I, López-Salmerón V et al (2019) Bifacial cambium stem cells generate xylem and phloem during radial plant growth. Development 146:dev171355
Smetana O, Mäkilä R, Lyu M et al (2019) High levels of auxin signalling define the stem-cell organizer of the vascular cambium. Nature 565:485–489
Soler M, Serra O, Molinas M et al (2007) A genomic approach to suberin biosynthesis and cork differentiation. Plant Physiol 144:419–431
Sundell D, Street NR, Kumar M et al (2017) AspWood: High-spatial-resolution rranscriptome profiles reveal uncharacterized modularity of wood formation in Populus tremula. Plant Cell 29:1585–1604
Teixeira RT, Fortes AM, Bai H et al (2018) Transcriptional profiling of cork oak phellogenic cells isolated by laser microdissection. Planta 247:317–338
Thamm A, Sanegre-Sans S, Paisley J et al (2019) A simple mathematical model of allometric exponential growth describes the early three-dimensional growth dynamics of secondary xylem in Arabidopsis roots. Roy Soc Open Sci 6:190126
Tian J, Chen J, Li B et al (2016) Association genetics in Populus reveals the interactions between Pto-miR160a and its target Pto-ARF16. Mol Genet Genomics 291:1069–1082
Todesco M, Balasubramanian S, Cao J et al (2012) Natural variation in biogenesis efficiency of individual Arabidopsis thaliana microRNAs. Curr Biol 22:166–170
Tuominen H, Puech L, Fink S et al (1997) A radial concentration gradient of indole-3-acetic acid is related to secondary xylem development in hybrid aspen. Plant Physiol 115:577–585
Uggla C, Moritz T, Sandberg G et al (1996) Auxin as a positional signal in pattern formation in plants. Proc Natl Acad Sci USA 93:9282–9286
Vulavala VK, Fogelman E, Faigenboim A et al (2019) The transcriptome of potato tuber phellogen reveals cellular functions of cork cambium and genes involved in periderm formation and maturation. Sci Rep 9:10216
Wang H, Avci U, Nakashima J et al (2010) Mutation of WRKY transcription factors initiates pith secondary wall formation and increases stem biomass in dicotyledonous plants. Proc Natl Acad Sci USA 107:22338–22343
Wang JW, Park MY, Wang LJ et al (2011) MicroRNA control of vegetative phase change in trees. PLoS Genet 2:e1002012
Wang C, Zhang S, Yu Y et al (2014) MiR397b regulates both lignin content and seed number in Arabidopsis via modulating a laccase involved in lignin biosynthesis. Plant Biotechnol J 12:1132–1142
Wareing PF (1958) Interaction between indole-acetic and gibberellic acid in cambial activity. Nature 181:1744–1745
Weigel D, Jurgens G (2002) Stem cells that make stems. Nature 415:751–754
Wu G, Poethig RS (2006) Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133:3539–3547
Wu G, Park MY, Conway SR et al (2009) The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138:750–759
Wunderling A, Ripper D, Barra-Jimenez A et al (2018) A molecular framework to study periderm formation in Arabidopsis. New Phytol 219:216–229
Xiao L, Quan M, Du Q et al (2017) Allelic Interactions among Pto-MIR475b and its four target genes potentially affect growth and wood properties in Populus. Front Plant Sci 8
Xu C, Shen Y, He F et al (2018) Auxin-mediated Aux/IAA-ARF-HB signaling cascade regulates secondary xylem development in Populus. New Phytol 222:752–767
Yang X, Du Q, Chen J et al (2015) Association mapping in Populus reveals the interaction between Pto-miR530a and its target Pto-KNAT1. Planta 242:77–95
Yoshida S, Barbier de Reuille P, Lane B et al (2014) Genetic control of plant development by overriding a geometric division rule. Dev Cell 29:75–87
Zhang Z, Zhang X (2012) Argonautes compete for miR165/166 to regulate shoot apical meristem development. Curr Opin Plant Biol 15:652–658
Zhao Y, Lin S, Qiu Z et al (2015) MicroRNA857 is involved in the regulation of secondary growth of vascular tissues in Arabidopsis. Plant Physiol 169:2539–2552
Zhong R, Ye ZH (1999) IFL1, a gene regulating interfascicular fiber differentiation in Arabidopsis encodes a homeodomain-leucine zipper protein. Plant Cell 11:2139–2152
Zhong R, Ye ZH (2004) Amphivasal vascular bundle 1, a gain-of-function mutation of the IFL1/REV gene, is associated with alterations in the polarity of leaves, stems and carpels. Plant Cell Physiol 45:369–385
Zhou G-K, Kubo M, Zhong R et al (2007) Overexpression of miR165 affects apical meristem formation, organ polarity establishment and vascular development in Arabidopsis. Plant Cell Physiol 48:391–404
Zhou Y, Honda M, Zhu H et al (2015) Spatiotemporal sequestration of miR165/166 by Arabidopsis argonaute10 promotes shoot apical meristem maintenance. Cell Rep 10:1819–1827
Zhu H, Hu F, Wang R et al (2011) Arabidopsis Argonaute10 specifically sequesters miR166/165 to regulate shoot apical meristem development. Cell 145:242–256
Zhu Y, Song D, Sun J (2013) PtrHB7, a class III HD-Zip gene, plays a critical role in regulation of vascular cambium differentiation in Populus. Mol Plant 6:1331–1343
Zhu Y, Song D, Xu P et al (2018) A HD-ZIP III gene, PtrHB4, is required for interfascicular cambium development in Populus. Plant Biotechnol J 16:808–817
Acknowledgements
The authors would like to thank funding from Fundação para a Ciência e Tecnologia, in the form of CEEC/IND/00175/2017 contract to Ana Milhinhos, Ph.D. fellowship PD/BD/114359/2016 to Susana Lopes, GREEN-it (grant no. UID/Multi/04551/2013) and BioISI (grant no. UID/Multi/04046/2019). The authors apologise to authors whose work could not be included in this review due to space limitations.
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Milhinhos, A., Lopes, S., Miguel, C. (2020). microRNA-Mediated Regulation of Plant Vascular Development and Secondary Growth. In: Miguel, C., Dalmay, T., Chaves, I. (eds) Plant microRNAs. Concepts and Strategies in Plant Sciences. Springer, Cham. https://doi.org/10.1007/978-3-030-35772-6_8
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