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Plant Growth Regulation

, Volume 86, Issue 2, pp 251–262 | Cite as

Temporal root responses in Arabidopsis thaliana L. to chromate reveal structural and regulatory mechanisms involving the SOLITARY ROOT/IAA14 repressor for maintenance of identity meristem genes

  • Fátima Hernández-Madrigal
  • Randy Ortiz-Castro
  • León Francisco Ruiz-Herrera
  • Carlos Cervantes
  • José López-Bucio
  • Miguel Martínez-Trujillo
Original paper
  • 73 Downloads

Abstract

The Arabidopsis root system is modified in response to stress generated by high concentrations of nonessential ions such as chromate [Cr(VI)]. In this work, the distribution of auxin and its transporters PIN1 and PIN7, as well as the expression of genes that maintain the identity of the root meristem, were analyzed in Arabidopsis thaliana wild-type (WT) seedlings and in a mutant affected in the SOLITARY ROOT (SLR1/IAA14) locus, which is required for root response to Cr(VI). We show that primary root inhibition, auxin transporter levels, and expression of meristem identity genes were maintained in the slr-1 mutants but not in WT plants in response to Cr(VI) in a time- and concentration-dependent manner. Notably, the outermost single cell layer of the lateral root cap, which normally dies and tends to peel off, remains viable and increases in size following exposure of WT plants, but not slr-1 mutants, to Cr(VI). Our results suggest that (1) the primary root tip senses Cr(VI), (2) the external lateral root cap may play a protective role during Cr(VI) exposure, and (3) Cr(VI) impacts cell division in root meristems via auxin redistribution and SLR1/IAA14 function, influencing the expression of root meristem genes.

Keywords

Chromate Root growth Meristem identity Auxin 

Notes

Funding

Funding was provided by Conacyt with Grant No. CB-2011-01-169769.

Supplementary material

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References

  1. Aichinger E, Kornet N, Friedrich T, Laux T (2012) Plant stem cell niches. Annu Rev Plant Biol 63:615–636CrossRefPubMedGoogle Scholar
  2. Aida M, Beis D, Heidstra R, Willemsen V, Blilou I, Galinha C, Nussaume L, Noh YS, Amasino R, Scheres B (2004) The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119:109–120CrossRefPubMedGoogle Scholar
  3. Arnaud C, Bonnot C, Desnos T, Nussaume L (2010) The root cap at the forefront. Criti Rev Biol 333:335–343Google Scholar
  4. Bellini C, Pacurar DI, Perrone I (2014) Adventitious roots and lateral roots: similarities and differences. Annu Rev Plant Biol 65:639–666CrossRefPubMedGoogle Scholar
  5. 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 119:57–70PubMedGoogle Scholar
  6. Benková E, Hejatko J (2009) Hormone interactions at the root apical meristem. Plant Mol Biol 69:383–396CrossRefPubMedGoogle Scholar
  7. Benková E, Michniewicz M, Sauer M, Teichmann T, Seifertová D, Jürgens G, Friml J (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115:591–602CrossRefGoogle Scholar
  8. Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J, Heidstra R, Aida M, Palme K, Scheres B (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433:39–44CrossRefGoogle Scholar
  9. 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 20:503–508CrossRefPubMedGoogle Scholar
  10. Dharmasiri N, Dharmasiri S, Estelle M (2005) The F-box protein TIR1 is an auxin receptor. Nature 435:441–445CrossRefPubMedGoogle Scholar
  11. Di Laurenzio L, Wysocka-Diller J, Malamy JE, Pysh L, Helariutta Y, Freshour G, Benfey PN (1996) The SCARECROW gene regulates an asymmetric cell division that is essential for generating the radial organization of the Arabidopsis Root. Cell 86:423–433CrossRefPubMedGoogle Scholar
  12. Dolan L, Janmaat K, Willemsen V, Linstead P, Poethig S, Roberts K, Scheres B (1993) Cellular organisation of the Arabidopsis thaliana root. Development 119:71–84PubMedGoogle Scholar
  13. Epstein E, Bloom AJ (2004) Mineral nutrition of plants: principles and perspectives, 2 edn. Sinnauer editorial, Sunderland, 400 ppGoogle Scholar
  14. Friml J (2003) Auxin transport—shaping the plant. Curr Opin Plant Biol 6:7–12CrossRefPubMedGoogle Scholar
  15. Fukaki H, Tameda S, Masuda H, Tasaka M (2002) Lateral root formation is blocked by a gain-of-function mutation in the SOLITARY-ROOT/IAA14 gene of Arabidopsis. Plant J 29:153–168CrossRefPubMedGoogle Scholar
  16. 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 449:1053–1057CrossRefPubMedGoogle Scholar
  17. Gray WM, del Pozo JC, Walker L, Hobbie L, Risseeuw E, Banks T, Crosby WL, Yang M, Ma H, Estelle M (1999) Identification of an SCF ubiquitin–ligase complex required for auxin response in Arabidopsis thaliana. Genes Dev 13:1678–1691CrossRefPubMedPubMedCentralGoogle Scholar
  18. Hayat S, Khalique G, Irfan M, Wani AS, Tripathi BN, Ahmad A (2012) Physiological changes induced by chromium stress in plants: an overview. Protoplasma 249:599–611CrossRefPubMedGoogle Scholar
  19. Holland SL, Avery SV (2011) Chromate toxicity and the role of sulfur. Metallomics 3:1119–1123CrossRefPubMedGoogle Scholar
  20. Kepinski S, Leyser O (2005) The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435:446–451CrossRefPubMedGoogle Scholar
  21. Kotaś J, Stasicka Z (2000) Chromium occurrence in the environment and methods of its speciation. Environ Pollut 107:263–283CrossRefPubMedGoogle Scholar
  22. Kumpf RP, Nowack MK (2015) The root cap: a short story of life and death. J Exp Bot 66:5651–5662CrossRefPubMedGoogle Scholar
  23. Lee Y, Lee WS, Kim SH (2013) Hormonal regulation of stem cell maintenance in roots. J Exp Bot 64:1153–1165CrossRefPubMedGoogle Scholar
  24. López-Bucio J, Ortiz-Castro R, Ruíz-Herrera LF, Juárez CV, Hernández-Madrigal F, Carreón-Abud Y, Martínez-Trujillo M (2015) Chromate induces adventitious root formation via auxin signalling and SOLITARY-ROOT/IAA14 gene function in Arabidopsis thaliana. Biometals 28:353–365CrossRefPubMedGoogle Scholar
  25. Lucas M, Swarup R, Paponov IA, Swarup K, Casimiro I, Lake D, Peret B, Zappala S, Mairhofer S, Whitword 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 155:384–398CrossRefPubMedGoogle Scholar
  26. Martínez-Trujillo M, Méndez-Bravo A, Ortiz-Castro R, Hernández-Madrigal F, Ibarra-Laclette E, Ruiz-Herrera LF, Long TA, Cervantes C, Herrera-Estrella L, López-Bucio J (2014) Chromate alters root system architecture and activates expression of genes involved in iron homeostasis and signaling in Arabidopsis thaliana. Plant Mol Biol 86:35–50CrossRefPubMedGoogle Scholar
  27. McGrath SP, Smith S (1990) Chromium and nickel. In: Alloway BJ (ed) Heavy Metals in soils. Wiley, New York, pp 125–150Google Scholar
  28. Mockaitis K, Estelle M (2008) Auxin receptors and plant development: a new signaling paradigm. Annu Rev Cell Dev Biol 24:55–80CrossRefPubMedGoogle Scholar
  29. Moubayidin L, Perilli S, Dello Ioio R, Di Mambro R, Costantino P, Sabatini S (2010) The rate of cell differentiation controls the arabidopsis root meristem growth phase. Curr Biol 20:1138–1143CrossRefPubMedGoogle Scholar
  30. Muday GK, DeLong A (2001) Polar auxin transport: controlling where and how much. Trends Plant Sci 6:535–542CrossRefPubMedGoogle Scholar
  31. Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497CrossRefGoogle Scholar
  32. Muto H, Watahiki MK, Nakamoto D, Kinjo M, Yamamoto KT (2007) Specificity and similarity of functions of the Aux/IAA genes in auxin signaling of Arabidopsis revealed by promoter-exchange experiments among MSG2/IAA19, AXR2/IAA7, and SLR/IAA14. Plant Physiol 144:187–196CrossRefPubMedPubMedCentralGoogle Scholar
  33. Ottenschläger I, Wolff P, Wolverton C, Bhalerao RP, Sandberg G, Ishikawa H, Evans M, Palme K (2003) Gravity-regulated differential auxin transport from columella to lateral root cap cells. Proc Natl Acad Sci USA 100:2987–2991CrossRefPubMedGoogle Scholar
  34. Péret B, Swarup K, Ferguson A, Seth M, Yang Y, Dhondt S, James N, Casimiro I, Perry P, Syed A, Yang H, Reemmer J, Venison E, Howells C, Prerez-Amador MA, Yung J, Alonso J, Beemster GTS, Laplaze L, Murphy A, Bennett MJ, Nielsen E, Swarup R (2012) AUX/LAX genes encode a family of auxin influx transporters that perform distinct functions during Arabidopsis development. Plant Cell 24:2874–2885CrossRefPubMedPubMedCentralGoogle Scholar
  35. Perilli S, Di Mambro R, Sabatini S (2012) Growth and development of the root apical meristem. Curr Opin Plant Biol 15:17–23CrossRefPubMedGoogle Scholar
  36. Perrot-Rechenmann C (2010) Cellular responses to auxin: division versus expansion. Cold Spring Harb Perspect Biol 2:a001446CrossRefPubMedPubMedCentralGoogle Scholar
  37. Petrášek J, Friml J (2009) Auxin transport routes in plant development. Development 136:2675–2688CrossRefPubMedGoogle Scholar
  38. Potters G, Pasternak TP, Guisez Y, Palme KJ, Jansen MAK (2007) Stress-induced morphogenic responses: growing out of trouble? Trends Plant Sci 12:98–105CrossRefPubMedGoogle Scholar
  39. Reed JW (2001) Roles and activities of Aux/IAA proteins in Arabidopsis. Trends Plant Sci 6:420–425CrossRefPubMedGoogle Scholar
  40. Ruiz-Herrera LF, Shane MW, López-Bucio J (2015) Nutritional regulation of root development. Wiley Interdiscip Rev: Dev Biol 4:431–443CrossRefGoogle Scholar
  41. Ruiz-Rosquete M, Barbez E, Kleine-Vehn J (2012) Cellular auxin homeostasis: gatekeeping is housekeeping. Mol Plant 5:772–786CrossRefGoogle Scholar
  42. Sabatini S, Beis D, Wolkenfelt H, Murfett J, Guilfoyle T, Malamy J, Benfey P, Leyser O, Bechtold N, Weisbeek P, Scheres B (1999) An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99:463–472CrossRefGoogle Scholar
  43. 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 17:354–358CrossRefPubMedPubMedCentralGoogle Scholar
  44. Scheres B, Benfey P, Dolan L (2002) Root development. The Arabidopsis Book. Am Soc Plant Biol 1:e0101Google Scholar
  45. Shani E, Salehin M, Zhang Y, Sanchez SE, Doherty C, Wang R, Mangado CC, Song L, Tal I, Pisanty O, Ecker JR, Kay SA, Pruneda-Paz J, Estelle M (2017) Plant stress tolerance requires auxin-sensitive Aux/IAA transcriptional repressors. Curr Biol 27:437–444CrossRefPubMedPubMedCentralGoogle Scholar
  46. Shanker AK, Cervantes C, Loza-Tavera H, Avudainayagam S (2005) Chromium toxicity in plants. Environ Int 31:739–753CrossRefPubMedGoogle Scholar
  47. Stepanova AN, Robertson-Hoyt J, Yun J, Benavente LM, Xie DY, Doležal K, Schleret A, Jürgens G, Alonso JM (2008) TAA1-Mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell 133:177–191CrossRefPubMedGoogle Scholar
  48. Tsugeki R, Fedoroff NV (1999) Genetic ablation of root cap cells in Arabidopsis. Proc Natl Acad Sci USA 96:12941–12946CrossRefPubMedGoogle Scholar
  49. Van den Berg C, Willemsen V, Hendriks G, Weisbeek P, Scheres B (1997) Short-range control of cell differentiation in the Arabidopsis root meristem. Nature 390:287–289CrossRefPubMedGoogle Scholar
  50. Vanneste S, Friml J (2009) Auxin: a trigger for change in plant development. Cell 136:1005–1016CrossRefPubMedGoogle Scholar
  51. Vieten A, Sauer M, Brewer PB, Friml J (2007) Molecular and cellular aspects of auxin-transport-mediated development. Trends Plant Sci 12:160–168CrossRefPubMedGoogle Scholar
  52. Viti C, Marchi E, Decorosi F, Giovannetti L (2014) Molecular mechanisms of Cr(VI) resistance in bacteria and fungi. FEMS Microbiol Rev 38:633–659CrossRefPubMedGoogle Scholar
  53. Weijers D, Benková E, Jäger KE, Schlereth A, Hamann T, Kientz M, Wilmoth J, Reed JW, Jürgens G (2005) Developmental specificity of auxin response by pairs of ARF and Aux/IAA transcriptional regulators. EMBO J 24:1874–1885CrossRefPubMedPubMedCentralGoogle Scholar
  54. Willemsen V, Bauch M, Bennett T, Campilho A, Wolkenfelt H, Xu J, Haseloff J, Scheres B (2008) The NAC domain transcription factors FEZ and SOMBRERO control the orientation of cell division plane in Arabidopsis root stem cells. Dev Cell 15:913–922CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Instituto de Investigaciones Químico-BiológicasUniversidad Michoacana de San Nicolás de HidalgoMoreliaMexico
  2. 2.CONACYT-Red de Estudios Moleculares AvanzadosInstituto de Ecología A. C.XalapaMexico
  3. 3.Facultad de BiologíaUniversidad Michoacana de San Nicolás de HidalgoMoreliaMexico

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