Abstract
In higher plants, the development of a mature embryo from the zygote follows a synchronized sequence of cell division, growth and differentiation events ultimately regulated by a highly coordinated gene expression. Several genome-wide expression studies during embryogenesis in Arabidopsis have been reported, including high-resolution single-cell directed, but current knowledge is mainly based on the coding transcriptome. Despite the available state-of-the-art technologies for transcriptome sequencing, there is still a gap in our understanding of the complex regulatory networks involving small non-coding RNAs. While a few microRNAs of specific conserved families have been functionally characterized, the role played by a major part of the microRNA population during the plant life cycle, including embryo development, in both model and non-model plants are yet to be discovered. In this chapter, we review the current knowledge of the gene expression regulation of plant embryogenesis by microRNAs, and discuss future perspectives for advancing our knowledge on plant embryo development in the light of the latest discoveries in this area.
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References
Armenta-Medina A, Lepe-soltero D, Xiang D, Datla R (2017) Arabidopsis thaliana miRNAs promote embryo pattern formation beginning in the zygote. Dev Biol 431:145–151
Axtell MJ (2013) Classification and comparison of small RNAs from plants. Annu Rev Plant Biol 64(1):137–159
Cairney J, Pullman GS (2007) The cellular and molecular biology of conifer embryogenesis. New Phytol 176:511–536
Cao M-J, Wang Z, Zhao Q, Mao JL, Speiser A, Wirtz M, Hell R, Zhu JK, Xiang CB (2014) Sulfate availability affects ABA levels and germination response to ABA and salt stress in Arabidopsis thaliana. Plant J 77:604–615
Chen J, Zeng B, Zhang M, Xie S, Wang G, Hauck A, Lai J (2014) Dynamic transcriptome landscape of maize embryo and endosperm development. Plant Physiol 166:252–264
Constabel CP, Yip L, Patton JJ, Christopher ME (2000) Polyphenol oxidase from hybrid poplar. Cloning and expression in response to wounding and herbivory. Plant Physiol 124:285–295
D’Ario M, Griffiths-Jones S, Kim M (2017) Small RNAs: big impact on plant development. Trends Plant Sci 22(12):1056–1068
Dastidar MG, Scarpa A, Magele I, Ruiz-Duarte P, Born P, Bald L, Jouannet V, Maizel A (2019) ARF5/MONOPTEROS directly regulates miR390 expression in Arabidopsis thaliana primary root meristem. Plant Direct https://doi.org/10.1101/463943
de Vega-Bartol J, Simões M, Lorenz WW, Rodrigues AS, Alba R, Dean JFD, Miguel C (2013) Transcriptomic analysis highlights epigenetic and transcriptional regulation during zygotic embryo development of Pinuspinaster. BMC Plant Biol 13:123
Dharmasiri N, Dharmasiri S, Weijers D, Lechner E, Yamada M, Hobbie L, Ehrismann JS, Jürgens G, Estelle M (2005) Plant development is regulated by a family of auxin receptor F box proteins. Dev Cell 9:109–119
Dong Z, Han MH, Fedoroff N (2008) The RNA-binding proteins HYL1 and SE promote accurate in vitro processing of pri-miRNA by DCL1. Proc Natl Acad Sci 105(29):9970–9975
Emery JF, Floyd SK, Alvarez J, Eshed Y, Hawker NP, Izhaki A, Baum SF, Bowman JL (2003) Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes. Curr Biol 13:1768–1774
Fang Y, Spector DL (2007) Identification of nuclear dicing bodies containing proteins for microRNA biogenesis in living Arabidopsis plants. Curr Biol 17(9):818–823
Goldberg RB, de Paiva G, Yadegari R (1994) Plant embryogenesis: zygote to seed. Science 266(5185):605–614
Gonçalves S, Cairney J, Maroco J, Oliveira MM, Miguel C (2005) Evaluation of control transcripts in real-time RT-PCR expression analysis during maritime pine embryogenesis. Planta 222:556–563
Grigg SP, Galinha C, Kornet N, Canales C, Scheres B, Tsiantis M (2009) Report repression of apical homeobox genes is required for embryonic root development in Arabidopsis. Curr Biol 19:1485–1490
Hakman I, von Arnold S (1985) Plantlet regeneration through somatic embryogenesis in Picea abies (Norway Spruce). J Plant Physiol 121(2):149–158
Hardtke CS, Ckurshumova W, Vidaurre DP, Singh S, Stamatiou G, Tiwari SB, Hagen G, Guilfoyle TJ, Berleth T (2004) Overlapping and non-redundant functions of the Arabidopsis auxin response factors MONOPTEROS and NONPHOTOTROPIC HYPOCOTYL 4. Development 131(5):1089–1100
He X, Shenkute AG, Wang W, Xu S (2018) Characterization of conserved and novel miRNAs in Lilium lancifolium Thunb. by high-throughput sequencing. Sci Rep 8:2880
Huang H, Long J, Zheng L, Li Y, Hu Y, Yu G et al (2016) Identification and characterization of microRNAs in maize endosperm response to exogenous sucrose using small RNA sequencing. Genomics 108:216–222
Hunter C, Willmann MR, Wu G, Yoshikawa M, Gutiérrez-Nava M, Poethig RS (2006) Trans-acting siRNA-mediated repression of ETTIN and ARF4 regulates heteroblasty in Arabidopsis. Development 133:2973–2981
Jagtap S, Shivaprasad PV (2014) Diversity, expression and mRNA targeting abilities of Argonaute-targeting miRNAs among selected vascular plants. BMC Genom 15:1049
Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14:787–799
Klimaszewska K, Hargreaves C, Trontin J (2016) Advances in conifer somatic embryogenesis since year 2000. In: Germana MA, Lambardi M (eds) In vitro embryogenesis in higher plants. Methods in molecular biology, vol 1359. Humana Press, New York
Knauer S, Holt AL, Rubio-Somoza I, Tucker EJ, Hinze A, Pisch M, Javelle M, Timmermans MC, Tucker MR, Laux T (2013) A protodermal miR394 signal defines a region of stem cell competence in the Arabidopsis shoot meristem. Dev Cell 24:125–132
Kou SJ, Wu XM, Liu Z, Liu YL, Xu Q, Guo WW (2012) Selection and validation of suitable reference genes for miRNA expression normalization by quantitative RT-PCR in citrus somatic embryogenic and adult tissues. Plant Cell Rep 31:2151–2163
Ledwoń A, Gaj MD (2009) LEAFY COTYLEDON2 gene expression and auxin treatment in relation to embryogenic capacity of Arabidopsis somatic cells. Plant Cell Rep 28:1677–1688
Li WF, Zhang SG, Han SY, Wu T, Zhang JH, Qi LW (2012) Regulation of LaMYB33 by miR159 during maintenance of embryogenic potential and somatic embryo maturation in Larixkaempferi (Lamb.) Carr Plant Cell Tissue Organ Cult 113(1):131–136
Li D, Wang L, Liu X, Cui D, Chen T, Zhang H, Jiang C, Xu C, Li P, Li S, Zhao L, Chen H (2013) Deep sequencing of maize small RNAs reveals a diverse set of microRNA in dry and imbibed seeds. PLoS ONE 8:1–14
Li ZX, Li SG, Zhang L, Han S, Li WF, Xu H, Yang W, Liu Y, Fan Y, Qi LW (2016) Over-expression of miR166a inhibits cotyledon formation in somatic embryos and promotes lateral root development in seedlings of Larix leptolepis. Plant Cell Tissue Organ Cult 127:461–473
Lin Y, Lai Z (2013) Comparative Analysis Reveals Dynamic Changes in miRNAs and Their Targets and Expression during Somatic Embryogenesis in Longan (Dimocarpus longan Lour.). PLoS ONE 8 (4):e60337
Lin Y, Lai Z, Tian Q, Lin L, Lai R, Yang M, Zhang D, Chen Y, Zhang Z (2015) Endogenous target mimics down-regulate miR160 mediation of ARF10, -16, and -17 cleavage during somatic embryogenesis in Dimocarpus longan Lour. Front Plant Sci 6:956
Liu PP, Montgomery TA, Fahlgren N, Kasschau KD, Nonogaki H, Carrington JC (2007) Repression of AUXIN RESPONSE FACTOR10 by microRNA160 is critical for seed germination and post-germination stages. Plant J 52:133–146
Liu X, Huang J, Wang Y, Khanna K, Xie Z, Owen H, Zhao D (2010) The role of floral organs in carpels, an Arabidopsis loss-of-function mutation in MicroRNA160a, in organogenesis and the mechanism regulating its expression. Plant J 62:416–428
Liu Q, Yao X, Pi L, Wang H, Cui X, Huang H (2009) The ARGONAUTE10 gene modulates shoot apical meristem maintenance and establishment of leaf polarity by repressing miR165/166 in Arabidopsis. Plant J 58 (1):27-40
Long JM, Liu CY, Feng MQ, Liu Y, Wu XM, Guo WW (2018) MiR156-SPL modules regulate induction of somatic embryogenesis in citrus callus. J Exp Bot 69:2979–2993
Luo YC, Zhou H, Li Y, Chen JY, Yang JH, Chen YQ, Qu LH (2006) Rice embryogeniccalli express a unique set of microRNAs, suggesting regulatory roles of microRNAs in plant post-embryogenic development. FEBS Lett 580:5111–5116
Mallory AC, Reinhart BJ, Jones-Rhoades MW, Tang G, Zamore PD, Barton MK, Bartel DP (2004) MicroRNA control of PHABULOSA in leaf development: importance of pairing to the microRNA 5′ region. EMBO J 23:3356–3364
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
Miguel CM, Rupps A, Raschke J, Rodrigues AS and Trontin JF (2016) Impact of molecular studies on somatic embryogenesis development for implementation in conifer multi-varietal forestry. In: Park YS, Bonga JM, Moon HK (eds) Vegetative propagation of forest trees. National Institute of Forest Science, pp 373–421
Miyashima S, Honda M, Hashimoto K, Tatematsu K, Hashimoto T, Sato-Nara K, Okada K, Nakajima K (2013) A comprehensive expression analysis of the Arabidopsis MICRORNA165/6 gene family during embryogenesis reveals a conserved role in meristem specification and a non-cell-autonomous function. Plant Cell Physiol 54(3):375–384
Möller BK, Hove CA, Xiang D, Williams N, López LG, Yoshida S, Smit M, Datla R, Weijers D (2017) Auxin response cell-autonomously controls ground tissue initiation in the early Arabidopsis embryo. PNAS 114(12):E2533–2539
Möller B, Weijers D (2009) Auxin control of embryo patterning. Cold Spring Harb Perspect Biol 1(5):a001545
Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, Estelle M, Voinnet O, Jones JD (2006) A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312:436–439
Nodine MD, Bartel DP (2010) MicroRNAs prevent precocious gene expression and enable pattern formation during plant embryogenesis. Genes Dev 24(23):2678–2692
Oh TJ, Wartell RM, Cairney J, Pullman GS (2008) Evidence for stage-specific modulation of specific microRNAs (miRNAs) and miRNA processing components in zygotic embryo and female gametophyte of loblolly pine (Pinus taeda). New Phytol 179:67–80
Palatnik JF, Allen E, Wu X, Schommer C, Schwab R, Carrington JC, Weigel D (2003) Control of leaf morphogenesis by microRNAs. Nature 425:257–263
Plotnikova A, Kellner MJ, Mosiolek M, Schon MA, Nodine MD (2019) MicroRNA dynamics and functions during Arabidopsis embryogenesis. Plant Cell https://doi.org/10.1105/tpc.19.00395
Pullman GS, Webb DT (1994) An embryo staging system for comparison of zygotic and somatic embryo development. In: Proceedings of the TAPPI R &D division biological sciences symposium, Minneapolis, MN, 3–6 Oct 1994. Technical Association of the Pulp and Paper Industry Press, Atlanta, pp 31–34
Rademacher EH, Möller B, Lokerse AS, Llavata-Peris CI, van den Berg W, Weijers D (2011) A cellular expression map of the Arabidopsis AUXIN RESPONSE FACTOR gene family. Plant J 68:597–606
Reichel A, Miller AA (2015) Specificity of plant miRNA target MIMIcs: Cross-targeting of miR1559 and miR319. J Plant Physiol 180:45–48
Ren L, Tang G (2012) Identification of sucrose-responsive microRNAs reveals sucroseregulated copper accumulations in an SPL7-dependent and independent manner in Arabidopsis thaliana. Plant Sci 187:59–68
Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel DP (2002) Prediction of plant microRNA targets. Cell 110:513–520
Rodrigues AR, Chaves I, Costa BV, Lin Y-C, Lopes S, Milhinhos A, Van de Peer Y, Miguel CM (2019) Small RNA profiling in Pinus pinaster reveals the transcriptome of developing seeds and highlights differences between zygotic and somatic embryos. Sci Rep 9:11327 https://doi.org/10.1038/s41598-019-47789-y
Schwartz BW, Yeung EC, Meinke DW (1994) Disruption of morphogenesis and transformation of the suspensor in abnormal suspensor mutants of Arabidopsis. Development 120:3235–3245
Seefried WF, Willmann MR, Clausen RL, Jenik PD (2014) Global regulation of embryonic patterning in Arabidopsis by MicroRNAs. Plant Physiol 165:670–687
Siddiqui ZH, Abbas ZK, Ansari MW, Khan MN (2018) The role of miRNA in somatic embryogenesis. Genomics 111(5):1026–1033
Singh H (1978) Embryology of gymnosperms. Encyclopedia of plant anatomy XII, Embryol gymnosperms Encycl plant Anat XII
Smertenko A, Bozhkov PV (2014) Somatic embryogenesis: life and death processes during apical-basal patterning. J Exp Bot 65(5):1343–1360
Smith ZR, Long JA (2010) Control of Arabidopsis apical–basal embryo polarity by antagonistic transcription factors. Nature 464:423–426
Smith SA, Beaulieu JM, Donoghue MJ (2010) An uncorrelated relaxed-clock analysis suggests an earlier origin for flowering plants. Proc Natl Acad Sci U S A 107:5897–5902
Su YH, Liu YB, Zhou C, Li XM, Zhang XS (2016) The miRNA167 controls somatic embryogenesis in Arabidopsis through regulating its target genes ARF6 and ARF8. Plant Cell Tiss Organ Cult 124:405–417
Szittya G, Moxon S, Santos MD, Jing R, Fevereiro MP, Moulton V, Dalmay T (2008) High-throughput sequencing of Medicago truncatula short RNAs identifies eight new miRNA families. BMC Genomics 9(1):593
Szyrajew K, Bielewicz D, Dolata J, Wójcik AM (2017) MicroRNAs are intensively regulated during induction of somatic embryogenesis in Arabidopsis. Front Plant Sci 8:1–16
Takada S, Hibara K, Ishida T, Tasaka M (2001) The CUP-SHAPED COTYLEDON1 gene of Arabidopsis regulates shoot apical meristem formation. Development 128:1127–1135
Takanashi H, Sumiyoshi H, Mogi M, Hayashi Y, Ohnishi T, Tsutsumi N (2018) miRNAs control HAM1 functions at the single-cell-layer level and are essential for normal embryogenesis in Arabidopsis. Plant Mol Biol 96:627–640
Tang X, Bian S, Tang M, Lu Q, Li S, Liu X, Tian G, Nguyen V, Tsang EWT, Wang A, Rothstein SJ, Chen X, Cui Y (2012) MicroRNA-mediated repression of the seed maturation program during vegetative development in Arabidopsis. PLoS Genet 8:20–22
ten Hove CA, Lu K-J, Weijers D (2015) Building a plant: cell fate specification in the early Arabidopsis embryo. Development 142:420–430
Vernoux T, Benfey PN (2005) Signals that regulate stem cell activity during plant development. Curr Opin Genet Dev 15:388–394
Vogel G (2005) How does a single somatic cell become a whole plant? Science 309:86
von Arnold S, Clapham D, Abrahamsson M (2019) Embryology in conifers. In: Cánovas FM (ed) Molecular physiology and biotechnology of trees. Advances in botanical research, vol 89. Elsevier, Amsterdam, pp 157–184
Wang JW, Wang LJ, Mao YB, Cai WJ, Xue HW, Chen XY (2005) Control of root cap formation by MicroRNA-targeted auxin response factors in Arabidopsis. Plant Cell 17:2204–2216
Wang J, Jian H, Wang T, Wei L, Li J, Li C, Liu L (2016) Identification of microRNAs actively involved in fatty acid biosynthesis in developing Brassica napus seeds using high-throughput sequencing. Front Plant Sci 7:1570
Weijers D, Schlereth A, Ehrismann JS, Schwank G, Kientz M, Jurgens G (2006) Auxin triggers transient local signaling for cell specification in Arabidopsis embryogenesis. Dev Cell 10(2):265–270
Wiggans SC (1954) Growth and organ formation in callus tissues derived from Daucus carota. Am J Botany 41(4):321
Willmann MR, Mehalick AJ, Packer RL, Jenik PD (2011) MicroRNAs regulate the timing of embryo maturation in Arabidopsis. Plant Physiol 155:1871–1884
Wójcik AM, Gaj MD (2016) miR393 contributes to the embryogenic transition induced in vitro in Arabidopsis via the modification of the tissue sensitivity to auxin treatment. Planta 244:231–243
Wójcik AM, Nodine MD, Gaj MD (2017) miR160 and miR166/165 contribute to the LEC2-mediated auxin response involved in the somatic embryogenesis induction in Arabidopsis. Front Plant Sci 8:1–17
Wu MF, Tian Q, Reed JW (2006) Arabidopsis microRNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction. Development 133:4211–4218
Wu XM, Liu MY, Ge XX, Xu Q, Guo WW (2011) Stage and tissue-specific modulation of ten conserved miRNAs and their targets during somatic embryogenesis of Valencia sweet orange. Planta 233:495–505
Wu XM, Kou SJ, Liu YL, Fang YN, Xu Q, Guo WW (2015) Genomewide analysis of small RNAs in nonembryogenic and embryogenic tissues of citrus: microRNA-and siRNA-mediated transcript cleavage involved in somatic embryogenesis. Plant Biotechnol J 13:383–394
Yakovlev IA, Fossdal CG (2017) In silico analysis of small RNAs suggest roles for novel and conserved miRNAs in the formation of epigenetic memory in somatic embryos of Norway spruce. Front Physiol 8:674
Yamasaki H, Hayashi M, Fukazawa M, Kobayashi Y, Shikanai T (2009) SQUAMOSA promoter binding protein-like7 is a central regulator for copper homeostasis in Arabidopsis. Plant Cell 21:347–361
Yang X, Wang L, Yuan D, Lindsey K, Zhang X (2013) Small RNA and degradome sequencing reveal complex miRNA regulation during cotton somatic embryogenesis. J Exp Bot 64:1521–1536
Yang T, Wang Y, Teotia S, Wang Z, Shi C, Sun H, Gu Y, Zhang Z, Tnag G (2019) The interaction between miR160 and miR165/ 166 in the control of leaf development and drought tolerance in Arabidopsis. Sci Rep 9:2832
Yao X, Chen J, Zhou J, Yu H, Ge C, Zhang M, Gao X, Dai X, Yang ZN, Zhao Y (2019) An essential role for miRNA167 in maternal control of embryonic and seed development. Plant Physiol 180:453–464
Yu B, Bi L, Zheng B, Ji L, Chevalier D, Agarwal M, Ramachandran V, Li W, Lagrange T, Walker JC, Chen X (2008) The FHA domain proteins DAWDLE in Arabidopsis and SNIP1 in humans act in small RNA biogenesis. ProcNatlAcadSci USA 105:10073–10078
Yu N, Niu QW, Ng KH, Chua NH (2015) The role of miR156/SPLs modules in Arabidopsis lateral root development. Plant J 83:673–685
Zhang S, Zhou J, Han S, Yang W, Li W, Wei H, Li X, Qi L (2010) Four abiotic stress-induced miRNA families differentially regulated in the embryogenic and non-embryogenic callus tissues of Larix leptolepis. Biochem Biophys Res Commun 398:355–360
Zhang J, Zhang S, Han S, Wu T, Li X, Li W, Qi L (2012) Genome-wide identification of microRNAs in larch and stage-specific modulation of 11 conserved microRNAs and their targets during somatic embryogenesis. Planta 236:647–657
Zhou Y, Liu X, Engstrom EM, Nimchuk ZL, Pruneda-Paz JL, Tarr PT, Yan A, Kay SA, Meyerowitz EM (2015) Control of plant stem cell function by conserved interacting transcriptional regulators. Nature 517:377–380
Zhu X, Lenf X, Sun X, Mu Q, Wang B, Li X, Wang C, Fang J (2015) Discovery of conservation and diversification of genes by phylogenetic analysis based on global genomes. Plant Genome 8(2)
Zimmerman JL (1993) Somatic embryogenesis: a model for early development in higher plants. Plant Cell 5(10):1411–1423
Zhang B, Wang Q (2015) MicroRNA-based Biotechnology for Plant Improvement. J Cell Physiol 230(1):1-15
Acknowledgements
We acknowledge the funding support provided by Fundaçãopara a Ciência e a Tecnologia (FCT), through grants UID/Multi/04046/2013 to BioISI (Biosystems and Integrative Sciences Institute)] and GREEN-it (UID/Multi/04551/2013), and the doctoral fellowships SFRH/BD/79779/2011 (to ASR) and SFRH/BD/128827/2017 (to AA).
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Alves, A., Rodrigues, A.S., Miguel, C. (2020). microRNAs in Plant Embryogenesis. 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_6
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