At-Hook Motif Nuclear Localised Protein 18 as a Novel Modulator of Root System Architecture

. 2020 Mar 10 ; 21 (5) : . [epub] 20200310

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid32164240

Grantová podpora
NPUI LO1417 Ministerstvo Školství, Mládeže a Tělovýchovy
410216 Grantová Agentura, Univerzita Karlova
A1-S-9236 Consejo Nacional de Ciencia y Tecnología
IN200818 Dirección General de Asuntos del Personal Académico, Universidad Nacional Autónoma de México

The At-Hook Motif Nuclear Localized Protein (AHL) gene family encodes embryophyte-specific nuclear proteins with DNA binding activity. They modulate gene expression and affect various developmental processes in plants. We identify AHL18 (At3G60870) as a developmental modulator of root system architecture and growth. AHL18 is involved in regulation of the length of the proliferation domain and number of dividing cells in the root apical meristem and thereby, cell production. Both primary root growth and lateral root development respond according to AHL18 transcription level. The ahl18 knock-out plants show reduced root systems due to a shorter primary root and a lower number of lateral roots. This change results from a higher number of arrested and non-developing lateral root primordia (LRP) rather than from a decreased LRP initiation. The over-expression of AHL18 results in a more extensive root system, longer primary roots, and increased density of lateral root initiation events. AHL18 is thus involved in the formation of lateral roots at both LRP initiation and their later development. We conclude that AHL18 participates in modulation of root system architecture through regulation of root apical meristem activity, lateral root initiation and emergence; these correspond well with expression pattern of AHL18.

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Malamy J.E., Benfey P.N. Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Development. 1997;124:33–44. PubMed

Torres-Martínez H.H., Rodríguez-Alonso G., Shishkova S., Dubrovsky J.G. Lateral Root Primordium Morphogenesis in Angiosperms. Front. Plant Sci. 2019;10 doi: 10.3389/fpls.2019.00206. PubMed DOI PMC

Banda J., Bellande K., von Wangenheim D., Goh T., Guyomarc’h S., Laplaze L., Bennett M.J. Lateral Root Formation in Arabidopsis: A Well-Ordered LRexit. Trends Plant Sci. 2019;24:826–839. doi: 10.1016/j.tplants.2019.06.015. PubMed DOI

Benitez-Alfonso Y., Faulkner C., Pendle A., Miyashima S., Helariutta Y., Maule A. Symplastic Intercellular Connectivity Regulates Lateral Root Patterning. Dev. Cell. 2013;26:136–147. doi: 10.1016/j.devcel.2013.06.010. PubMed DOI

Vermeer J.E.M., von Wangenheim D., Barberon M., Lee Y., Stelzer E.H.K., Maizel A., Geldner N. A Spatial Accommodation by Neighboring Cells Is Required for Organ Initiation in Arabidopsis. Science. 2014;343:178–183. doi: 10.1126/science.1245871. PubMed DOI

Marhavý P., Montesinos J.C., Abuzeineh A., Van Damme D., Vermeer J.E.M., Duclercq J., Rakusová H., Nováková P., Friml J., Geldner N., et al. Targeted cell elimination reveals an auxin-guided biphasic mode of lateral root initiation. Genes Dev. 2016;30:471–483. doi: 10.1101/gad.276964.115. PubMed DOI PMC

Benkova E., Michniewicz M., Sauer M., Teichmann T., Seifertova D., Jurgens G., Friml J. Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell. 2003;115:591–602. doi: 10.1016/S0092-8674(03)00924-3. PubMed DOI

Dubrovsky J.G., Sauer M., Napsucialy-Mendivil S., Ivanchenko M.G., Friml J., Shishkova S., Celenza J., Benková E. Auxin acts as a local morphogenetic trigger to specify lateral root founder cells. Proc. Natl. Acad. Sci. USA. 2008;105:8790–8794. doi: 10.1073/pnas.0712307105. PubMed DOI PMC

Péret B., De Rybel B., Casimiro I., Benková E., Swarup R., Laplaze L., Beeckman T., Bennett M.J. Arabidopsis lateral root development: An emerging story. Trends Plant Sci. 2009;14:399–408. doi: 10.1016/j.tplants.2009.05.002. PubMed DOI

Okushima Y., Fukaki H., Onoda M., Theologis A., Tasaka M. ARF7 and ARF19 regulate lateral root formation via direct activation of LBD/ASL genes in Arabidopsis. Plant Cell. 2007;19:118–130. doi: 10.1105/tpc.106.047761. PubMed DOI PMC

Motte H., Vanneste S., Beeckman T. Molecular and Environmental Regulation of Root Development. Annu. Rev. Plant Biol. 2019:465–488. doi: 10.1146/annurev-arplant-050718-100423. PubMed DOI

Lavenus J., Goh T., Guyomarc’H S., Hill K., Lucas M., Voß U., Kenobi K., Wilson M.H., Farcot E., Hagen G., et al. Inference of the arabidopsis lateral root gene regulatory network suggests a bifurcation mechanism that defines primordia flanking and central zones. Plant Cell. 2015;27:1368–1388. doi: 10.1105/tpc.114.132993. PubMed DOI PMC

Zhao J., Favero D.S., Peng H., Neff M.M. Arabidopsis thaliana AHL family modulates hypocotyl growth redundantly by interacting with each other via the PPC/DUF296 domain. Proc. Natl. Acad. Sci. USA. 2013;110:E4688–E4697. doi: 10.1073/pnas.1219277110. PubMed DOI PMC

Fujimoto S., Matsunaga S., Yonemura M., Uchiyama S., Azuma T., Fukui K. Identification of a novel plant MAR DNA binding protein localized on chromosomal surfaces. Plant Mol. Biol. 2004;56:225–239. doi: 10.1007/s11103-004-3249-5. PubMed DOI

Wong M.M., Bhaskara G.B., Wen T.N., Lin W.D., Nguyen T.T., Chong G.L., Verslues P.E. Phosphoproteomics of Arabidopsis Highly ABA-Induced1 identifies AT-Hook-Like10 phosphorylation required for stress growth regulation. Proc. Natl. Acad. Sci. USA. 2019;116:2354–2363. doi: 10.1073/pnas.1819971116. PubMed DOI PMC

Ng K.-H., Yu H., Ito T. AGAMOUS Controls GIANT KILLER, a Multifunctional Chromatin Modifier in Reproductive Organ Patterning and Differentiation. PLoS Biol. 2009;7:e1000251. doi: 10.1371/journal.pbio.1000251. PubMed DOI PMC

Lim P.O., Kim Y., Breeze E., Koo J.C., Woo H.R., Ryu J.S., Park D.H., Beynon J., Tabrett A., Buchanan-Wollaston V., et al. Overexpression of a chromatin architecture-controlling AT-hook protein extends leaf longevity and increases the post-harvest storage life of plants. Plant J. 2007;52:1140–1153. doi: 10.1111/j.1365-313X.2007.03317.x. PubMed DOI

Yun J., Kim Y.S., Jung J.H., Seo P.J., Park C.M. The AT-hook motif-containing protein AHL22 regulates flowering initiation by modifying FLOWERING LOCUS T chromatin in Arabidopsis. J. Biol. Chem. 2012;287:15307–15316. doi: 10.1074/jbc.M111.318477. PubMed DOI PMC

Lu H., Zou Y., Feng N. Overexpression of AHL20 negatively regulates defenses in arabidopsis. J. Integr. Plant Biol. 2010;52:801–808. doi: 10.1111/j.1744-7909.2010.00969.x. PubMed DOI

Yadeta K.A., Hanemian M., Smit P., Hiemstra J.A., Pereira A., Marco Y., Thomma B.P.H.J. DNA-Binding Protein AHL19 Mediates Verticillium Wilt Resistance. Mol. Plant Microbe Interact. 2011;24:1582–1591. doi: 10.1094/MPMI-04-11-0090. PubMed DOI

Howden A.J.M., Stam R., Martinez Heredia V., Motion G.B., ten Have S., Hodge K., Marques Monteiro Amaro T.M., Huitema E. Quantitative analysis of the tomato nuclear proteome during Phytophthora capsici infection unveils regulators of immunity. New Phytol. 2017;215:309–322. doi: 10.1111/nph.14540. PubMed DOI PMC

Street I.H., Shah P.K., Smith A.M., Avery N., Neff M.M. The AT-hook-containing proteins SOB3/AHL29 and ESC/AHL27 are negative modulators of hypocotyl growth in Arabidopsis. Plant J. 2008;54:1–14. doi: 10.1111/j.1365-313X.2007.03393.x. PubMed DOI

Matsushita A., Furumoto T., Ishida S., Takahashi Y. AGF1, an AT-hook protein, is necessary for the negative feedback of AtGA3ox1 encoding GA 3-oxidase. Plant Physiol. 2007;143:1152–1162. doi: 10.1104/pp.106.093542. PubMed DOI PMC

Lee K., Seo P.J. Coordination of matrix attachment and ATP-dependent chromatin remodeling regulate auxin biosynthesis and Arabidopsis hypocotyl elongation. PLoS ONE. 2017;12 doi: 10.1371/journal.pone.0181804. PubMed DOI PMC

Zhou J., Wang X., Lee J.-Y., Lee J.-Y. Cell-to-Cell Movement of Two Interacting AT-Hook Factors in Arabidopsis Root Vascular Tissue Patterning. Plant Cell. 2013;25:187–201. doi: 10.1105/tpc.112.102210. PubMed DOI PMC

Xiao C., Chen F., Yu X., Lin C., Fu Y.-F. Over-expression of an AT-hook gene, AHL22, delays flowering and inhibits the elongation of the hypocotyl in Arabidopsis thaliana. Plant Mol. Biol. 2009;71:39–50. doi: 10.1007/s11103-009-9507-9. PubMed DOI

Sundaresan V., Springer P., Volpe T., Haward S., Jones J.D.G., Dean C., Ma H., Martienssen R. Patterns of gene action in plant development revealed by enhancer trap and gene trap transposable elements. Genes Dev. 1995;9:1797–1810. doi: 10.1101/gad.9.14.1797. PubMed DOI

Vielle-Calzada J.P., Baskar R., Grossniklaus U. Delayed activation of the paternal genome during seed development. Nature. 2000;404:91–94. doi: 10.1038/35003595. PubMed DOI

Liu Y.-G., Chen Y., Zhang Q. Amplification of Genomic Sequences Flanking T-DNA Insertions by Thermal Asymmetric Interlaced Polymerase Chain Reaction. Methods Mol. Biol. 2005;286:341–348. PubMed

Deuschle K., Chaudhuri B., Okumoto S., Lager I., Lalonde S., Frommer W.B. Rapid Metabolism of Glucose Detected with FRET Glucose Nanosensors in Epidermal Cells and Intact Roots of Arabidopsis RNA-Silencing Mutants. Plant Cell Online. 2006;18:2314–2325. doi: 10.1105/tpc.106.044073. PubMed DOI PMC

Dubrovsky J.G., Fordeb B.G. Quantitative analysis of lateral root development: Pitfalls and how to avoid them. Plant Cell. 2012;24:4–14. doi: 10.1105/tpc.111.089698. PubMed DOI PMC

Ivanov V.B., Dubrovsky J.G. Estimation of the cell-cycle duration in the root apical meristem: A model of linkage between cell-cycle duration, rate of cell production, and rate of root growth. Int. J. Plant Sci. 1997;158:757–763. doi: 10.1086/297487. DOI

Napsucialy-Mendivil S., Dubrovsky J.G. Genetic and Phenotypic Analysis of Lateral Root Development in Arabidopsis thaliana. Methods Mol. Biol. 2018;1761:47–75. PubMed

Jiang H., Moreno-Romero J., Santos-González J., De Jaeger G., Gevaert K., Van De Slijke E., Köhler C. Ectopic application of the repressive histone modification H3K9me2 establishes post-zygotic reproductive isolation in Arabidopsis Thaliana. Genes Dev. 2017;31:1272–1287. doi: 10.1101/gad.299347.117. PubMed DOI PMC

Yin D., Liu X., Shi Z., Li D., Zhu L. An AT-hook protein DEPRESSED PALEA1 physically interacts with the TCP Family transcription factor RETARDED PALEA1 in rice. Biochem. Biophys. Res. Commun. 2018;495:487–492. doi: 10.1016/j.bbrc.2017.11.031. PubMed DOI

Zhou L., Liu Z., Liu Y., Kong D., Li T., Yu S., Mei H., Xu X., Liu H., Chen L., et al. A novel gene OsAHL1 improves both drought avoidance and drought tolerance in rice. Sci. Rep. 2016;6:30264. doi: 10.1038/srep30264. PubMed DOI PMC

Rodríguez J., Mosquera J., Couceiro J.R., Vázquez M.E., Mascareñas J.L. The AT-Hook motif as a versatile minor groove anchor for promoting DNA binding of transcription factor fragments. Chem. Sci. 2015;6:4767–4771. doi: 10.1039/C5SC01415H. PubMed DOI PMC

Greb T., Lohmann J.U. Plant Stem Cells. Curr. Biol. 2016;26:R816–R821. doi: 10.1016/j.cub.2016.07.070. PubMed DOI

Gruel J., Landrein B., Tarr P., Schuster C., Refahi Y., Sampathkumar A., Hamant O., Meyerowitz E.M., Jönsson H. An epidermis-driven mechanism positions and scales stem cell niches in plants. Sci. Adv. 2016;2:22–24. doi: 10.1126/sciadv.1500989. PubMed DOI PMC

Ma J., Liu Y., Zhou W., Zhu Y., Dong A., Shen W.H. Histone chaperones play crucial roles in maintenance of stem cell niche during plant root development. Plant J. 2018;95:86–100. doi: 10.1111/tpj.13933. PubMed DOI

Mähönen A.P., Bishopp A., Higuchi M., Nieminen K.M., Kinoshita K., Törmäkangas K., Ikeda Y., Oka A., Kakimoto T., Helariutta Y. Cytokinin signaling and its inhibitor AHP6 regulate cell fate during vascular development. Science. 2006;311:94–98. doi: 10.1126/science.1118875. PubMed DOI

Harashima H., Schnittger A. The integration of cell division, growth and differentiation. Curr. Opin. Plant Biol. 2010;13:66–74. doi: 10.1016/j.pbi.2009.11.001. PubMed DOI

Serrano-Mislata A., Schiessl K., Sablowski R. Active Control of Cell Size Generates Spatial Detail during Plant Organogenesis. Curr. Biol. 2015;25:2991–2996. doi: 10.1016/j.cub.2015.10.008. PubMed DOI PMC

Tian Q., Reed J.W. Control of auxin-regulated root development by the Arabidopsis thaliana SHY2/IAA3 gene. Development. 1999;126:711–721. PubMed

Moubayidin L., Perilli S., Dello Ioio R., Di Mambro R., Costantino P., Sabatini S. The rate of cell differentiation controls the arabidopsis root meristem growth phase. Curr. Biol. 2010;20:1138–1143. doi: 10.1016/j.cub.2010.05.035. PubMed DOI

Ivanov V.B., Dubrovsky J.G. Longitudinal zonation pattern in plant roots: Conflicts and solutions. Trends Plant Sci. 2013;18:237–243. doi: 10.1016/j.tplants.2012.10.002. PubMed DOI

Di Mambro R., De Ruvo M., Pacifici E., Salvi E., Sozzani R., Benfey P.N., Busch W., Novak O., Ljung K., Di Paola L., et al. Auxin minimum triggers the developmental switch from cell division to cell differentiation in the Arabidopsis root. Proc. Natl. Acad. Sci. USA. 2017;114:E7641–E7649. doi: 10.1073/pnas.1705833114. PubMed DOI PMC

Di Mambro R., Svolacchia N., Dello Ioio R., Pierdonati E., Salvi E., Pedrazzini E., Vitale A., Perilli S., Sozzani R., Benfey P.N., et al. The Lateral Root Cap Acts as an Auxin Sink that Controls Meristem Size. Curr. Biol. 2019;29:1199–1205. doi: 10.1016/j.cub.2019.02.022. PubMed DOI

Napsucialy-Mendivil S., Alvarez-Venegas R., Shishkova S., Dubrovsky J.G. Arabidopsis homolog of trithorax1 (ATX1) is required for cell production, patterning, and morphogenesis in root development. J. Exp. Bot. 2014;65:6373–6384. doi: 10.1093/jxb/eru355. PubMed DOI PMC

Aida M., Beis D., Heidstra R., Willemsen V., Blilou I., Galinha C., Nussaume L., Noh Y.-S., Amasino R., Scheres B. The PLETHORA Genes Mediate Patterning of the Arabidopsis Root Stem Cell Niche. Cell. 2004;119:109–120. doi: 10.1016/j.cell.2004.09.018. PubMed DOI

Tsukagoshi H., Busch W., Benfey P.N. Transcriptional Regulation of ROS Controls Transition from Proliferation to Differentiation in the Root. Cell. 2010;143:606–616. doi: 10.1016/j.cell.2010.10.020. PubMed DOI

Yang L., Zhang J., He J., Qin Y., Hua D., Duan Y., Chen Z., Gong Z. ABA-Mediated ROS in Mitochondria Regulate Root Meristem Activity by Controlling PLETHORA Expression in Arabidopsis. PLoS Genet. 2014;10:e1004791. doi: 10.1371/journal.pgen.1004791. PubMed DOI PMC

Yu Q., Tian H., Yue K., Liu J., Zhang B., Li X., Ding Z. A P-Loop NTPase Regulates Quiescent Center Cell Division and Distal Stem Cell Identity through the Regulation of ROS Homeostasis in Arabidopsis Root. PLOS Genet. 2016;12:e1006175. doi: 10.1371/journal.pgen.1006175. PubMed DOI PMC

Péret B., Larrieu A., Bennett M.J. Lateral root emergence: A difficult birth. J. Exp. Bot. 2009;60:3637–3643. doi: 10.1093/jxb/erp232. PubMed DOI

Dubrovsky J.G., Doerner P.W., Colón-Carmona A., Rost T.L. Pericycle cell proliferation and lateral root initiation in Arabidopsis. Plant Physiol. 2000;124:1648–1657. doi: 10.1104/pp.124.4.1648. PubMed DOI PMC

Parizot B., Laplaze L., Ricaud L., Boucheron-Dubuisson E., Bayle V., Bonke M., De Smet I., Poethig S.R., Helariutta Y., Haseloff J., et al. Diarch symmetry of the vascular bundle in arabidopsis root encompasses the pericycle and is reflected in distich lateral root initiation. Plant Physiol. 2008;146:140–148. doi: 10.1104/pp.107.107870. PubMed DOI PMC

Beeckman T., Burssens S., Inze D. The peri-cell-cycle in Arabidopsis. J. Exp. Bot. 2001;52:403–411. PubMed

Nieuwland J., Maughan S., Dewitte W., Scofield S., Sanz L., Murray J.A.H. The D-type cyclin CYCD4;1 modulates lateral root density in Arabidopsis by affecting the basal meristem region. Proc. Natl. Acad. Sci. USA. 2009;106:22528–22533. doi: 10.1073/pnas.0906354106. PubMed DOI PMC

Lloret P.G., Casero P.J., Pulgarín A., Navascués J. The Behaviour of Two Cell Populations in the Pericycle of Allium cepa, Pisum sativum, and Daucus carota During Early Lateral Root Development. Ann. Bot. 1989;63:465–475. doi: 10.1093/oxfordjournals.aob.a087767. DOI

Lavrekha V.V., Pasternak T., Ivanov V.B., Palme K., Mironova V.V. 3D analysis of mitosis distribution highlights the longitudinal zonation and diarch symmetry in proliferation activity of the Arabidopsis thaliana root meristem. Plant J. 2017;92:834–845. doi: 10.1111/tpj.13720. PubMed DOI

Celenza J.L., Grisafi P.L., Fink G.R. A pathway for lateral root formation in Arabidopsis thaliana. Genes Dev. 1995;9:2131–2142. doi: 10.1101/gad.9.17.2131. PubMed DOI

DiDonato R.J., Arbuckle E., Buker S., Sheets J., Tobar J., Totong R., Grisafi P., Fink G.R., Celenza J.L. Arabidopsis ALF4 encodes a nuclear-localized protein required for lateral root formation. Plant J. 2004;37:340–353. doi: 10.1046/j.1365-313X.2003.01964.x. PubMed DOI

Alarcón M.V., Salguero J., Lloret P.G. Auxin modulated initiation of lateral roots is linked to pericycle cell length in Maize. Front. Plant Sci. 2019;10:1–10. doi: 10.3389/fpls.2019.00011. PubMed DOI PMC

Goh T., Toyokura K., Wells D.M., Swarup K., Yamamoto M., Mimura T., Weijers D., Fukaki H., Laplaze L., Bennett M.J., et al. Quiescent center initiation in the Arabidopsis lateral root primordia is dependent on the SCARECROW transcription factor. Development. 2016;143:3363–3371. doi: 10.1242/dev.135319. PubMed DOI

Du Y., Scheres B. Lateral root formation and the multiple roles of auxin. J. Exp. Bot. 2018;69:155–167. doi: 10.1093/jxb/erx223. PubMed DOI

Laskowski M.J., Williams M.E., Nusbaum H.C., Sussex I.M. Formation of lateral root meristems is a two-stage process. Development. 1995;121:3303–3310. PubMed

Tian H., De Smet I., Ding Z. Shaping a root system: Regulating lateral versus primary root growth. Trends Plant Sci. 2014;19:426–431. doi: 10.1016/j.tplants.2014.01.007. PubMed DOI

Shimotohno A., Heidstra R., Blilou I., Scheres B. Root stem cell niche organizer specification by molecular convergence of PLETHORA and SCARECROW transcription factor modules. Genes Dev. 2018;32:1085–1100. doi: 10.1101/gad.314096.118. PubMed DOI PMC

de Smet I., White P.J., Glyn Bengough A., Dupuy L., Parizot B., Casimiro I., Heidstra R., Laskowski M., Lepetit M., Hochholdinger F., et al. Analyzing lateral root development: How to move forward. Plant Cell. 2012;24:15–20. doi: 10.1105/tpc.111.094292. PubMed DOI PMC

Swarup K., Benková E., Swarup R., Casimiro I., Péret B., Yang Y., Parry G., Nielsen E., De Smet I., Vanneste S., et al. The auxin influx carrier LAX3 promotes lateral root emergence. Nat. Cell Biol. 2008;10:946–954. doi: 10.1038/ncb1754. PubMed DOI

Dubrovsky J.G., Gambetta G.A., Hernández-Barrera A., Shiskova S., Gonzáles I. Lateral Root Initiation in Arabidopsis: Developmental Window, Spatial Patterning, Density and Predictability. Ann. Bot. 2006;97:903–915. doi: 10.1093/aob/mcj604. PubMed DOI PMC

Lobet G., Pagès L., Draye X. A Novel Image-Analysis Toolbox Enabling Quantitative Analysis of Root System Architecture. Plant Physiol. 2011;157:29–39. doi: 10.1104/pp.111.179895. PubMed DOI PMC

Murray M.G., Thompson W.F. Nucleic Acids Research Rapid Isolation of High Molecular Weight Plant DNA. Nucleic Acids Res. 1980;8:4321–4326. doi: 10.1093/nar/8.19.4321. PubMed DOI PMC

Ramakers C., Ruijter J.M., Deprez R.H.L., Moorman A.F.M. Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci. Lett. 2003;339:62–66. doi: 10.1016/S0304-3940(02)01423-4. PubMed DOI

Soukup A. Selected Simple Methods of Plant Cell Wall Histochemistry and Staining for Light Microscopy. Humana Press; Totowa, NJ, USA: 2014. pp. 25–40. PubMed

Kotogány E., Dudits D., Horváth G.V., Ayaydin F. A rapid and robust assay for detection of S-phase cell cycle progression in plant cells and tissues by using ethynyl deoxyuridine. Plant Methods. 2010;6:1–15. doi: 10.1186/1746-4811-6-5. PubMed DOI PMC

NCSS . NCSS 9 Statistical Software No Title 2013. NCSS LLC; Kaysville, UT, USA: 2013.

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