Advertisement

Protoplasma

pp 1–10 | Cite as

Determinate root development in the halted primary root1 mutant of Arabidopsis correlates with death of root initial cells and an enhanced auxin response

  • Javier Raya-González
  • Randy Ortiz-Castro
  • José López-BucioEmail author
Original Article
  • 61 Downloads

Abstract

The transit from indeterminate to determinate root developmental program compromises growth and causes the differentiation of the meristem, but a direct link between this process with auxin signaling and/or viability of initial cells remains untested. Here, through the isolation and characterization of the halted primary root1 (hpr1) mutant of Arabidopsis, which develops primary and lateral roots with genetically stable determinate growth after germination, we show that the differentiation of the root meristem correlates with enhanced auxin responsiveness and is preceded by the death of provasculature initial cells in both primary and lateral roots. Supplementation of indole-3-acetic acid causes both a dose-dependent repression of primary root growth and an induction of DR5:uidA expression in wild-type seedlings, and these effects were exacerbated in hpr1 mutants. The damage of provasculature initial cells in the root of hpr1 mutants occurred at earlier times than the full differentiation of the meristem, and correlates with a reduced expression domain of CycB1:uidA and PRZ:uidA. Thus, HPR1 plays critical functions for stem cell maintenance, auxin homeostasis, cell division in the meristem, and indeterminate root growth.

Keywords

Root stem cells Determinate root growth Cell viability Auxin Arabidopsis thaliana 

Notes

Acknowledgments

We appreciate the generosity of Drs. Philip Benfey, Christian Luschnig, and Tom Guilfoyle for providing materials and the kind support of Drs. Bonnie Bartel and Bethany K. Zolman for recombination mapping of HPR1.

Funding information

This study received funding from the Coordinación de la Investigación Científica UMSNH (México) via project 2.26 (JLB).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

709_2019_1409_Fig7_ESM.png (1 mb)
Supplementary figure 1

Germination and initial root establishment of WT and hpr1 mutants. Germination at 24 and 48 h after stratification of WT and hpr1 seeds (n = 100). (b) Representative images of germinating seedlings showing the normal protrusion of the root. Scale bars represent 0.5 cm. The experiment was repeated three times with similar results. Scale bar represent 0.5 cm. (PNG 1033 kb)

709_2019_1409_MOESM1_ESM.tif (2.9 mb)
High Resolution image (TIF 2957 kb)
709_2019_1409_Fig8_ESM.png (430 kb)
Supplementary figure 2

Expression of DR5:uidA in WT and hpr1 shoots. Representative images of 10 d-old seedlings showing auxin-inducible DR5:uidA expression. 10 seedlings were histochemically processed to show GUS expression. The experiment was repeated three times with similar results. Scale bar represent 0.5 cm. (PNG 429 kb)

709_2019_1409_MOESM2_ESM.tif (1.4 mb)
High Resolution image (TIF 1437 kb)

References

  1. Ayala-Rodríguez JA, Barrera-Ortiz S, Ruiz-Herrera LF, López-Bucio J (2017) Folic acid orchestrates root development linking cell elongation with auxin response and acts independently of the TARGET OF RAPAMYCIN signaling in Arabidopsis thaliana. Plant Sci 264:168–178CrossRefGoogle Scholar
  2. Bell CJ, Ecker JR (1994) Assignment of 30 microsatellite loci to the linkage map of Arabidopsis. Genomics 19:137–144CrossRefGoogle Scholar
  3. Benfey PN, Linstead PJ, Roberts K, Schiefelbein JW, Hauser MT, Aeschbacher RA (1993) Root development in Arabidopsis: four mutants with dramatically altered root morphogenesis. Development 119:57–70Google Scholar
  4. Brumos J, Robles LM, Yun J, Vu TC, Jackson S, Alonso JM, Stepanova AN (2018) Local auxin biosynthesis is a key regulator of plant development. Dev Cell 47:306–318CrossRefGoogle Scholar
  5. Colón-Carmona A, You R, Haimovitch-Gal T, Doerner P (1999) Spatio-temporal analysis of mitotic activity with a labile cyclin–GUS fusion protein. Plant J 20:503–508CrossRefGoogle Scholar
  6. Fulcher N, Sablowski R (2009) Hypersensitivity to DNA damage in plant stem cell niches. Proc Natl Acad Sci U S A 106:20984–20988CrossRefGoogle Scholar
  7. 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 449:1053–1057CrossRefGoogle Scholar
  8. Hayashi K, Hasegawa J, Matsunaga S (2013) The boundary of the meristematic and elongation zones in roots: endoreduplication precedes rapid cell expansion. Sci Rep 3:2723CrossRefGoogle Scholar
  9. Jia N, Liu X, Gao H (2016) A DNA2 homolog is required for DNA damage repair, cell cycle regulation, and meristem maintenance in plants. Plant Physiol 171:318–333CrossRefGoogle Scholar
  10. Konieczny A, Ausubel FM (1993) A procedure for mapping Arabidopsis mutations using co-dominant ecotype-specific PCR-based markers. Plant J 4:403–410CrossRefGoogle Scholar
  11. López-Bucio J, Cruz-Ramırez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol 6:280–287CrossRefGoogle Scholar
  12. Lucas M, Swarup R, Paponov IA, Swarup K, Casimiro I, Lake D, Peret B, Zappala S, Mairhofer S, Whitworth M, Wang J, Ljung K, Marchant A, Sandberg G, Holdsworth MJ, Palme K, Pridmore T, Mooney S, Bennett MJ (2011) SHORT-ROOT regulates primary, lateral, and adventitious root development in Arabidopsis. Plant Physiol 155:384–398CrossRefGoogle Scholar
  13. Malamy JE, Benfey PN (1997) Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Development 124:33–44Google Scholar
  14. Méndez-Bravo A, Ruiz-Herrera LF, Cruz-Ramírez A, Guzman P, Martínez-Trujillo M, Ortiz-Castro R, López-Bucio J (2019) CONSTITUTIVE TRIPLE RESPONSE1 and PIN2 act in a coordinate manner to support the indeterminate root growth and meristem cell proliferating activity in Arabidopsis seedlings. Plant Sci 280:175–186CrossRefGoogle Scholar
  15. Petricka JJ, Winter CM, Benfey PN (2012) Control of Arabidopsis root development. Annu Rev Plant Biol 63:563–590CrossRefGoogle Scholar
  16. Raya-González J, Oropeza-Aburto A, López-Bucio JS, Guevara-García AA, de Veylder L, López-Bucio J, Herrera-Estrella L (2018) MEDIATOR18 influences Arabidopsis root architecture, represses auxin signaling and is a critical factor for cell viability in root meristems. Plant J 96:895–909CrossRefGoogle Scholar
  17. Reyes-Hernández BJ, Srivastava AC, Ugartechea-Chirino Y, Shishkova S, Ramos-Parra PA, Lira-Ruan V, Díaz de la Garza RI, Dong G, Moon JC, Blancaflor EB, Dubrovsky JG (2014) The root indeterminacy-to-determinacy developmental switch is operated through a folate-dependent pathway in Arabidopsis thaliana. New Phytol 202:1223–1236CrossRefGoogle Scholar
  18. Ruiz Herrera LF, Shane MW, López-Bucio J (2015) Nutritional regulation of root development. Wiley Interdiscip Rev Dev Biol 4:431–443CrossRefGoogle Scholar
  19. Sánchez-Calderón L, López-Bucio J, Chacón-López A, Cruz-Ramírez A, Nieto-Jacobo F, Dubrovsky J, Herrera-Estrella L (2005) Phosphate starvation induces a determinate developmental program in the roots of Arabidopsis thaliana. Plant Cell Physiol 46:174–184CrossRefGoogle Scholar
  20. Shishkova S, Rost TL, Dubrovsky JG (2008) Determinate root growth and meristem maintenance in angiosperms. Ann Bot 101:319–340CrossRefGoogle Scholar
  21. Sieberer T, Hauser MT, Seifert GJ, Luschnig C (2003) PROPORZ1, a putative Arabidopsis transcriptional adaptor protein, mediates auxin and cytokinin signals in the control of cell proliferation. Curr Biol 13:837–842CrossRefGoogle Scholar
  22. Smith S, De Smet I (2012) Root system architecture: insights from Arabidopsis and cereal crops. Philos Trans R Soc B 367:1441–1452CrossRefGoogle Scholar
  23. Timilsina R, Kim JH, Nam HG, Woo HR (2019) Temporal changes in cell division rate and genotoxic stress tolerance in quiescent center cells of Arabidopsis primary root apical meristem. Sci Rep 9:3599CrossRefGoogle Scholar
  24. Ulmasov T, Murfett J, Hagen G, Guilfoyle T (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9:1963–1971Google Scholar
  25. Xiong Y, McCormack M, Li L, Hall Q, Xiang C, Sheen J (2013) Glucose-TOR signalling reprograms the transcriptome and activates meristems. Nature 496:181–186CrossRefGoogle Scholar
  26. Zhang QQ, Li Y, Fu ZY, Liu XB, Yuan K, Fang Y, Liu Y, Li G, Zhang XS, Chong K, Ge L (2018) Intact Arabidopsis RPB1 functions in stem cell niches maintenance and cell cycling control. Plant J 95:150–167CrossRefGoogle Scholar
  27. Zhou W, Lozano-Torres JL, Blilou I, Zhang X, Zhai Q, Smant G, Li C, Scheres B (2019) A jasmonate signaling network activates root stem cells and promotes regeneration. Cell 177:942–956.e14.  https://doi.org/10.1016/j.cell.2019.03.006 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Instituto de Investigaciones Químico-BiológicasUniversidad Michoacana de San Nicolás de HidalgoMoreliaMexico
  2. 2.Facultad de Químico FarmacobiologíaUniversidad Michoacana de San Nicolás de HidalgoMoreliaMexico
  3. 3.Catedrático CONACYT-Instituto de Ecología, A.C., Red de Estudios Moleculares AvanzadosXalapaMexico

Personalised recommendations