Skip to main content
SpringerLink
Log in

Apical meristem exhaustion during determinate primary root growth in the moots koom 1 mutant of Arabidopsis thaliana

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

An indeterminate developmental program allows plant organs to grow continuously by maintaining functional meristems over time. The molecular mechanisms involved in the maintenance of the root apical meristem are not completely understood. We have identified a new Arabidopsis thaliana mutant named moots koom 1 (mko1) that showed complete root apical meristem exhaustion of the primary root by 9 days post-germination. MKO1 is essential for maintenance of root cell proliferation. In the mutant, cell division is uncoupled from cell growth in the region corresponding to the root apical meristem. We established the sequence of cellular events that lead to meristem exhaustion in this mutant. Interestingly, the SCR and WOX5 promoters were active in the mko1 quiescent center at all developmental stages. However, during meristem exhaustion, the mutant root tip showed defects in starch accumulation in the columella and changes in auxin response pattern. Therefore, contrary to many described mutants, the determinate growth in mko1 seedlings does not appear to be a consequence of incorrect establishment or affected maintenance of the quiescent center but rather of cell proliferation defects both in stem cell niche and in the rest of the apical meristem. Our results support a model whereby the MKO1 gene plays an important role in the maintenance of the root apical meristem proliferative capacity and indeterminate root growth, which apparently acts independently of the SCR/SHR and WOX5 regulatory pathways.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

CLSM:

Confocal Laser Scanning Microscopy

dag:

Days after germination

DMSO:

Dimethyl sulfoxide

EMS:

Ethyl methanesulfonate

GFP:

Green fluorescent protein

MS:

Murashige and Skoog medium

QC:

Quiescent center

RAM:

Root apical meristem

SSLP:

Simple Sequence Length Polymorphism

mko1 :

moots koom 1

References

  • Aida M, Beis D, Heidstra R, Willemsen V, Blilou I, Galinha C, Nussaume L, Noh Y-S, Amasino R, Scheres B (2004) The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119:109–120

    Article  PubMed  CAS  Google Scholar 

  • Azpeitia E, Benitez M, Vega I, Villarreal C, Alvarez-Buylla ER (2010) Single-cell and coupled GRN models of cell patterning in the Arabidopsis thaliana root stem cell niche. BMC Syst Biol 4:134

    Article  PubMed  Google Scholar 

  • Barlow PW (1976) Towards an understanding of the behaviour of root meristems. J Theor Biol 57:433–451

    Article  PubMed  CAS  Google Scholar 

  • Baum SF (1996) The developmental organization of the root apical meristem in Arabidopsis thaliana CV WS. Ph.D. dissertation, University of California, Davis, CA, USA

  • Baum SF, Rost TL (1996) Root apical organization in Arabidopsis thaliana 1. Root cap and protoderm. Protoplasma 192:178–188

    Article  Google Scholar 

  • Baum SF, Dubrovsky JG, Rost TL (2002) Apical organization and maturation of the cortex and vascular cylinder in Arabidopsis thaliana (Brassicaceae) roots. Am J Bot 89:908–920

    Article  PubMed  Google Scholar 

  • Benfey P, Linstead PJ, Roberts K, Schiefelbein JW, Hauser MT, Aeschbacher RA (1993) Root development in Arabidopsis: four mutants with dramatically altered root morphogenesis. Development 119:57–70

    PubMed  CAS  Google Scholar 

  • Benková E, Ivanchenko MG, Friml J, Shishkova S, Dubrovsky JG (2009) A morphogenetic trigger: is there an emerging concept in plant developmental biology? Trends Plant Sci 14:189–193

    Article  PubMed  Google Scholar 

  • Bennett T, Scheres B (2010) Root development-two meristems for the price of one? Curr Top Dev Biol 91:67

    Article  PubMed  CAS  Google Scholar 

  • Blilou I, Frugier F, Folmer S, Serralbo O, Willemsen V, Wolkenfelt H, Eloy NB, Ferreira PCG, Weisbeek P, Scheres B (2002) The Arabidopsis HOBBIT gene encodes a CDC27 homolog that links the plant cell cycle to progression of cell differentiation. Genes Dev 16:2566–2575

    Article  PubMed  CAS  Google Scholar 

  • Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml I, Heidstra R, Aida M, Palme K, Scheres B (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433:39–44

    Article  PubMed  CAS  Google Scholar 

  • Cheng JC, Seeley KA, Sung ZR (1995) RML1 and RML2, Arabidopsis genes required for cell proliferation at the root tip. Plant Physiol 107:365–376

    Article  PubMed  CAS  Google Scholar 

  • Colón-Carmona A, You R, Haimovitch-Gal T, Doerner P (1999) Technical advance: spatio-temporal analysis of mitotic activity with a labile cyclin–GUS fusion protein. Plant J 20:503–508

    Article  PubMed  Google Scholar 

  • Cui H, Levesque MP, Vernoux T, Jung JW, Paquette AJ, Gallagher KL, Wang JY, Blilou I, Scheres B, Benfey PN (2007) An evolutionarily conserved mechanism delimiting SHR movement defines a single layer of endodermis in plants. Science 316:421–425

    Article  PubMed  CAS  Google Scholar 

  • Ding Z, Friml J (2010) Auxin regulates distal stem cell differentiation in Arabidopsis roots. Proc Natl Acad Sci USA 107:12046–12051

    Article  PubMed  CAS  Google Scholar 

  • Dolan L, Janmaat K, Willemsen V, Linstead P, Poethig S, Roberts K, Scheres B (1993) Cellular organisation of the Arabidopsis thaliana root. Development 119:71–84

    PubMed  CAS  Google Scholar 

  • Drenkard E, Richter BG, Rozen S, Stutius LM, Angell NA, Mindrinos M, Cho RJ, Oefner PJ, Davis RW, Ausubel FM (2000) A simple procedure for the analysis of single nucleotide polymorphisms facilitates map-based cloning in Arabidopsis. Plant Physiol 124:1483–1492

    Article  PubMed  CAS  Google Scholar 

  • Dubrovsky JG (1997) Determinate primary-root growth in seedlings of Sonoran Desert Cactaceae; its organization, cellular basis, and ecological significance. Planta 203:85–92

    CAS  Google Scholar 

  • Dubrovsky JG, Soukup A, Napsucialy-Mendivil S, Jeknic Z, Ivanchenko MG (2009) The lateral root initiation index: an integrative measure of primordium formation. Ann Bot 103:807–817

    Article  PubMed  CAS  Google Scholar 

  • Friml J, Vieten A, Sauer M, Weijers D, Schwarz H, Hamann T, Offringa R, Jürgens G (2003) Efflux-dependent auxin gradients establish the apical–basal axis of Arabidopsis. Nature 426:147–153

    Article  PubMed  CAS  Google Scholar 

  • Galinha C, Hofhuis H, Luijten M, Willemsen V, Blilou I, Heidstra R, Scheres B (2007) PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development. Nature 449:1053–1057

    Article  PubMed  CAS  Google Scholar 

  • Hamann T, Mayer U, Jürgens G (1999) The auxin-insensitive bodenlos mutation affects primary root formation and apical-basal patterning in the Arabidopsis embryo. Development 126:1387–1395

    PubMed  CAS  Google Scholar 

  • Hamann T, Benková E, Bäurle I, Kientz M, Jürgens G (2002) The Arabidopsis BODENLOS gene encodes an auxin response protein inhibiting MONOPTEROS-mediated embryo patterning. Genes Dev 16:1610–1615

    Article  PubMed  CAS  Google Scholar 

  • Hardtke CS, Ckurshumova W, Vidaurre DP (2004) Overlapping and non- redundant functions of the Arabidopsis auxin response factors MONOPTEROS and NONPHOTOTROPIC HYPOCOTYL 4. Development 131:1089–1100

    Article  PubMed  CAS  Google Scholar 

  • Helariutta Y, Fukaki H, Wysocka-Diller J, Nakajima K, Jung J, Sena G, Hauser MT, Benfey PN (2000) The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling. Cell 101:555–567

    Article  PubMed  CAS  Google Scholar 

  • Ivanov VB (1974) Kletochnye Osnovy Rosta Rastenii (Cellular Bases of Plant Growth). Nauka, Moscow (in Russian)

  • Ivanov VB (1994) Root growth responses to chemicals. Sov Sci Rev D Physicochem Biol 13:1–70

    Google Scholar 

  • Ivanov VB, Dobrochaev AE, Baskin TI (2002) What the distribution of cell lengths in the root meristem does and does not reveal about cell division. J Plant Growth Regul 21:60–67

    Article  PubMed  CAS  Google Scholar 

  • Jiang K, Meng YL, Feldman LJ (2003) Quiescent center formation in maize roots is associated with an auxin-regulated oxidizing environment. Development 130:1429–1438

    Article  PubMed  CAS  Google Scholar 

  • Jiang K, Zhu T, Diao Z, Huang H, Feldman LJ (2010) The maize root stem cell niche: a partnership between two sister cell populations. Planta 231:411–424

    Article  PubMed  CAS  Google Scholar 

  • Kidner C, Sundaresan V, Roberts K, Dolan L (2000) Clonal analysis of the Arabidopsis root confirms that position, not lineage, determines cell fate. Planta 211:191–199

    Article  PubMed  CAS  Google Scholar 

  • Koprivova A, Mugford ST, Kopriva S (2010) Arabidopsis root growth dependence on glutathione is linked to auxin transport. Plant Cell Rep 29:1157–1167

    Article  PubMed  CAS  Google Scholar 

  • Lukowitz W, Gillmor CS, Scheible WR (2000) Positional cloning in Arabidopsis. Why it feels good to have a genome initiative working for you. Plant Physiol 123:795–805

    Article  PubMed  CAS  Google Scholar 

  • Nakajima K, Sena G, Nawy T, Benfey PN (2001) Intercellular movement of the putative transcription factor SHR in root patterning. Nature 413:307–311

    Article  PubMed  CAS  Google Scholar 

  • Overvoorde P, Fukaki H, Beeckman T (2010) Auxin control of root development. Cold Spring Harb Perspect Biol 2:a001537

    Article  PubMed  Google Scholar 

  • Pérez-Pérez JM, Serralbo O, Vanstraelen M, González C, Criqui MC, Genschik P, Kondorosi E, Scheres B (2008) Specialization of CDC27 function in the Arabidopsis thaliana anaphase-promoting complex (APC/C). Plant J 53:78–89

    Article  PubMed  Google Scholar 

  • Reddy GV, Heisler MG, Ehrhardt DW, Meyerowitz EM (2004) Real-time lineage analysis reveals oriented cell divisions associated with morphogenesis at the shoot apex of Arabidopsis thaliana. Development 131:4225–4237

    Article  PubMed  CAS  Google Scholar 

  • Rodríguez-Rodríguez JF, Shishkova S, Napsucialy-Mendivil S, Dubrovsky JG (2003) Apical meristem organization and lack of establishment of the quiescent center in Cactaceae roots with determinate growth. Planta 217:849–857

    Article  PubMed  Google Scholar 

  • Sabatini S, Beis D, Wolkenfelt H, Murfett J, Guilfoyle T, Malamy J, Benfey J, Leyser O, Bechtold N, Weisbeek P, Scheres B (1999) An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99:463–472

    Article  PubMed  CAS  Google Scholar 

  • Sabatini S, Heidstra R, Wildwater M, Scheres B (2003) SCARECROW is involved in positioning the stem cell niche in the Arabidopsis root meristem. Genes Dev 17:354–358

    Article  PubMed  CAS  Google Scholar 

  • Sarkar AK, Luijten M, Miyashima S, Lenhard M, Hashimoto T, Nakajima K, Scheres R, Heidstra R, Laux T (2007) Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446:811–814

    Article  PubMed  CAS  Google Scholar 

  • Scheres B, Wolkenfelt H, Willemsen V, Terlouw M, Lawson E, Dean C, Weisbeek P (1994) Embryonic origin of the Arabidopsis primary root and root meristem initials. Development 120:2475–2487

    CAS  Google Scholar 

  • Serralbo O, Pérez-Pérez JM, Heidstra R, Scheres B (2006) Non-cell-autonomous rescue of anaphase-promoting complex function revealed by mosaic analysis of HOBBIT, an Arabidopsis CDC27 homolog. Proc Natl Acad Sci USA 103:13250–13255

    Article  PubMed  CAS  Google Scholar 

  • Shishkova S, Dubrovsky JG (2005) Developmental programmed cell death in primary roots of Sonoran Desert Cactaceae. Am J Bot 92:1590–1594

    Article  PubMed  Google Scholar 

  • Shishkova S, Rost TL, Dubrovsky JG (2008) Determinate root growth and meristem maintenance in angiosperms. Ann Bot 101:319–340

    Article  PubMed  CAS  Google Scholar 

  • Stahl Y, Wink RH, Ingram GC, Simon R (2009) A signaling module controlling the stem cell niche in Arabidopsis root meristems. Curr Biol 19:909–914

    Article  PubMed  CAS  Google Scholar 

  • Truernit E, Bauby H, Dubreucq B, Grandjean O, Runions J, Barthelemy J, Palauqui JC (2008) High-resolution whole-mount imaging of three-dimensional tissue organization and gene expression enables the study of phloem development and structure in Arabidopsis. Plant Cell 20:1494–1503

    Article  PubMed  CAS  Google Scholar 

  • Ueda M, Matsui K, Ishiguro S, Sano R, Wada T, Paponov I, Palme K, Okada K (2004) The HALTED ROOT gene encoding the 26S proteasome subunit RPT2a is essential for the maintenance of Arabidopsis meristems. Development 131:2101–2111

    Article  PubMed  CAS  Google Scholar 

  • van den Berg C, Willemsen V, Hage W, Weisbeek P, Scheres B (1995) Cell fate in the Arabidopsis root meristem determined by directional signalling. Nature 378:62–65

    Article  PubMed  Google Scholar 

  • van den Berg C, Willemsen W, Hendriks G, Weisbeek P, Scheres B (1997) Short-range control of cell differentiation in the Arabidopsis root meristem. Nature 390:287–289

    Article  PubMed  Google Scholar 

  • Vanneste S, Friml J (2009) Auxin: a trigger for change in plant development. Cell 136:1005–1016

    Article  PubMed  CAS  Google Scholar 

  • Vanstraelen M, Baloban M, Da Ines O, Cultrone A, Lammens T, Boudolf V, Brown SC, De Veylder L, Mergaert P, Kondorosi E (2009) APC/C −CCS52A complexes control meristem maintenance in the Arabidopsis root. Proc Natl Acad Sci USA 106:11806–11811

    Article  PubMed  CAS  Google Scholar 

  • Vernoux T, Wilson RC, Seeley KA, Reichheld JP, Muroy S, Brown S, Maughan SC, Cobbett CS, Van Montagu M, Inzé D, May MJ, Sung ZR (2000) The ROOT MERISTEMLESS1/CADMIUM SENSITIVE2 gene defines a glutathione-dependent pathway involved in initiation and maintenance of cell division during postembryonic root development. Plant Cell 12:97–110

    Article  PubMed  CAS  Google Scholar 

  • Von Guttenberg H (1960) Grundzüge der Histogenese höherer Pflanzen. I. Die Angiospermen. Gebruder Borntraeger, Berlin

    Google Scholar 

  • Willemsen V, Wolkenfelt H, de Vrieze G, Weisbeek P, Scheres B (1998) The HOBBIT gene is required for formation of the root meristem in the Arabidopsis embryo. Development 125:521–531

    PubMed  CAS  Google Scholar 

  • Wysocka-Diller JW, Helariutta Y, Fukaki H, Malamy JE, Benfey PN (2000) Molecular analysis of SCARECROW function reveals a radial patterning mechanism common to root and shoot. Development 127:595–603

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank J. M. Hurtado-Ramírez, S. Ainsworth, E. López, P, Gaitan, M. E. Salas-Ocampo, G. Zavala-Padilla, and A. M. Saralegui for excellent technical help, P. Doerner, B. Scheres, J. Friml, and K. Okada for seed donation and A. Colón-Carmona for critical reading of a previous version of the manuscript. The research was supported by the Dirección General de Asuntos del Personal Académico (DGAPA)—Programa de Apoyo a Proyectos de Investigación e Innovación Tecnológica, Universidad Nacional Autónoma de México (grant IN212509 to S.S. and grants IN225906 and IN212009 to J.G.D.), Consejo Nacional de Ciencia y Technología (CONACyT), Mexico (grant 79736 to S.S. and grants 49267 and 127957 to J.G.D.). Doctorate fellowship to A.H.-B. from CONACyT and postdoctoral fellowship from DGAPA-UNAM (to G.D., V.L.-R., A.S., and Y.U.-C.) are gratefully acknowledged.

Author information

Author notes

  1. Aleš Soukup

    Present address: Department of Plant Physiology, Charles University in Prague, Vinična 5, 128 44, Prague, Czech Republic

  2. Verónica Lira-Ruan

    Present address: Laboratorio de Fisiología y Desarrollo Vegetal, Facultad de Ciencias, Universidad Autónoma del Estado de Morelos, Av. Universidad 1001 Col. Chamilpa, 62209, Cuernavaca, Morelos, Mexico

  3. Gaofeng Dong

    Present address: Division of Basic Biomedical Sciences, Sanford School of Medicine, University of South Dakota, Vermillion, SD, 57069, USA

Authors and Affiliations

  1. Departamento de Biología Molecular de Plantas, Instituto de Biotecnología, Universidad Nacional Autónoma de México, Apartado Postal 510-3, 62250, Cuernavaca, Morelos, Mexico

    Alejandra Hernández-Barrera, Yamel Ugartechea-Chirino, Svetlana Shishkova, Selene Napsucialy-Mendivil, Aleš Soukup, Blanca Jazmín Reyes-Hernández, Verónica Lira-Ruan, Gaofeng Dong & Joseph G. Dubrovsky

Authors
  1. Alejandra Hernández-Barrera
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yamel Ugartechea-Chirino
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Svetlana Shishkova
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Selene Napsucialy-Mendivil
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Aleš Soukup
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Blanca Jazmín Reyes-Hernández
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Verónica Lira-Ruan
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Gaofeng Dong
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Joseph G. Dubrovsky
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Joseph G. Dubrovsky.

Additional information

A. Hernández-Barrera and Y. Ugartechea-Chirino contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

425_2011_1470_MOESM1_ESM.tif

Suppl. Material S1. Map location of mko1. The MKO1 locus is positioned on the lower arm of chromosome IV between SSLP markers CER453190 and CER460296. The mapped interval includes 2.7 Mb. The number of recombination events per the number of scored chromosomes for each marker and marker position are shown. The open circle indicates the centromere. The CCS52A2 (7.1 Mb), RML1 (12.1 Mb) and SHR (17. 6 Mb) loci are outside the mapping region. (TIFF 429 kb)

Suppl. Material S2 (DOC 63 kb)

425_2011_1470_MOESM3_ESM.tif

Suppl. Material S3 Representative morphological features of cell differentiation in mko1 primary RAM with completely exhausted RAM. Median longitudinal sections of cleared (a, b) and pseudo-Schiff-stained (c, d) roots. Scanning electron microscopy image of the root apex (e). The mko1 exhausted meristem is characterized by the following features: mature xylem strands (arrowheads in a and b) and root hairs (white arrows in a, b, and e) or root hair bulges (yellow arrow in b) near the root apex; swollen or abnormally elongated epidermal cells (c, d). Mutant root tips with exhausted RAM can maintain a remnant root cap (c) or consist of elongated cells in the position of the root cap (d). Scale bar 20 μm (a, b) and 50 μm (c-e) (TIFF 6449 kb)

425_2011_1470_MOESM4_ESM.tif

Suppl. Material S4 pWOX5::GFP expression is not restricted to the QC in wild-type and the mko1 mutant. Median longitudinal sections of pWOX5::GFP (a, b) and mko1 pWOX5::GFP (c, d) stem cell niche. GFP signal capture was obtained at the same conditions in 3- and 6-dag seedlings, and the images were enhanced post-capture using ImageJ software to facilitate visualization of the GFP distribution. When pWOX5::GFP is expressed at 3 dag in the wild-type background, GFP signal is mainly restricted to the QC (a) and is subsequently expanded to the surrounding initials by 6 dag (b). In the mko1 background, the GFP signal is relatively less restricted to the QC in 3- (c) and 6 (d)-dag seedlings (corresponding to stages I and II of the RAM exhaustion). Scale bar 20 μm (TIFF 788 kb)

425_2011_1470_MOESM5_ESM.tif

Suppl. Material S5 Cell growth impairment in mko1 mutant cortex cells early after germination (1 dag). Cortical cell length at fixed cell positions within the meristematic region; cell number one is a daughter cell of the cortex-endodermis initial. Mean ± SE, n = 5 (wild type) and 7 (mko1) roots with two cells measured per root at each position (TIFF 1189 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hernández-Barrera, A., Ugartechea-Chirino, Y., Shishkova, S. et al. Apical meristem exhaustion during determinate primary root growth in the moots koom 1 mutant of Arabidopsis thaliana . Planta 234, 1163–1177 (2011). https://doi.org/10.1007/s00425-011-1470-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-011-1470-4

Keywords

Search

Navigation