Skip to main content
Log in

Sucrose Protects Arabidopsis Roots from Chromium Toxicity Influencing the Auxin–Plethora Signaling Pathway and Improving Meristematic Cell Activity

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Plants adapt to challenging growth conditions, such as the scarcity of nutrients or exposure to toxic metals, via changes in root system architecture. Chromium (Cr) is a non-essential element that when supplied in sublethal concentrations inhibits primary root growth through decreasing meristematic activity and affects photosynthesis. Here, we show that sucrose reverses the inhibitory effects of Cr(VI) on plant growth and development. Sucrose supplementation reactivated primary root growth under repressing Cr(VI) concentrations by restoring cell division and auxin distribution at the root meristem, keeping stem cell niche functioning. Analysis of the growth of Arabidopsis wild-type and mutant seedlings defective in auxin transport or signaling further revealed a critical role of auxin in mediating the effects of sucrose to protect plants from Cr(VI) toxicity. The results suggest that sucrose acts as a regulator in the maintenance of root meristem activity to overcome the stress generated by sublethal Cr(VI) concentrations.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Aichinger E, Kornet N, Friedrich T, Laux T et al (2012) Plant stem cell niches. Annu Rev Plant Biol 63:615–636

    Article  CAS  PubMed  Google Scholar 

  • Aida M, Beis D, Heidstra R, Willemsen V, Blilou I, et al (2004) The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119:109–120

    Article  CAS  PubMed  Google Scholar 

  • Atkinson NJ, Urwin PE (2012) The interaction of plant biotic and abiotic stresses: from genes to the field. J Exp Bot 63:3523–3543

    Article  CAS  PubMed  Google Scholar 

  • Benková E, Hejatko J (2009) Hormone interactions at the root apical meristem. Plant Mol Biol 69:383–396

    Article  PubMed  Google Scholar 

  • 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 433:39–44

    Article  CAS  PubMed  Google Scholar 

  • Cervantes C, Campos-García J, Devars S, Gutiérrez-Corona F, Tavera HL, Torres-Guzmán JC, Moreno-Sánchez R (2001) Interactions of chromium with microorganisms and plants. FEMS Microbiol Rev 25:335–347

    Article  CAS  PubMed  Google Scholar 

  • Chaudhuri B, Hörmann F, Lalonde S, Brady SM, Orlando DA, Benfey P, Frommer WB (2008) Protonophore-and pH-insensitive glucose and sucrose accumulation detected by FRET nanosensors in Arabidopsis root tips. Plant J 56:948–962

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen LQ, Qu XQ, Hou BH, Sosso D, Osorio S, Fernie AR, Frommer WB (2012) Sucrose efflux mediated by SWEET proteins as a key step for phloem transport. Science 335:207–211

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Davies PJ (2004) Plant hormones: biosynthesis, signal transduction, action! Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Dharmasiri N, Dharmasiri S, Estelle M (2005) The F-box protein TIR1 is an auxin receptor. Nature 435:441–445

    Article  CAS  PubMed  Google Scholar 

  • 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 29:153–168

    Article  CAS  PubMed  Google Scholar 

  • Gälweiler L, Guan C, Müller A, Wisman E, Mendgen K, Yephremov A, Palme K (1998) Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282:2226–2230

    Article  PubMed  Google Scholar 

  • Gottwald JR, Krysan PJ, Young JC, Evert RF, Sussman MR (2000) Genetic evidence for the in planta role of phloem-specific plasma membrane sucrose transporters. Proc Natl Acad Sci USA 7:13979–13984

    Article  Google Scholar 

  • Imlau A, Truernit E, Sauer N (1999) Cell-to-cell and long-distance trafficking of the green fluorescent protein in the phloem and symplastic unloading of the protein into sink tissues. Plant Cell 11:309–322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson MP (2016) Photosynthesis. Essays Biochem 60:255–273

    Article  PubMed  PubMed Central  Google Scholar 

  • Kepinski S, Leyser O (2005) The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435:446–451

    Article  CAS  PubMed  Google Scholar 

  • Krecek P, Skupa P, Libus J, Naramoto S, Tejos R, Friml J, Zazímalová E (2009) The PIN-FORMED (PIN) protein family of auxin transporters. Genome Biol 10(249):1–11

    Google Scholar 

  • Lalonde S, Wipf D, Frommer WB (2004) Transport mechanisms for organic forms of carbon and nitrogen between source and sink. Annu Rev Plant Biol 55:341–372

    Article  CAS  PubMed  Google Scholar 

  • Li SB, Xie ZZ, Hu CG, Zhang JZ (2016) A review of auxin response factors (ARFs) in plants. Front Plant Sci 7(47):1–6

    Google Scholar 

  • Lilley JLS, Gee CW, Sairanen I, Ljung K, Nemhauser JL (2012) An endogenous carbon-sensing pathway triggers increased auxin flux and hypocotyl elongation. Plant Physiol 160:2261–2270

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin XY, Ye YQ, Fan SK, Jin CW, Shao Jian S, Zheng SJS (2015) Increased sucrose accumulation regulates iron-deficiency responses by promoting auxin signalling in Arabidopsis plants. Plant Physiol 170:907–920

    Article  PubMed  PubMed Central  Google Scholar 

  • Lincoln C, Britton JH, Estelle M (1990) Growth and development of the axr1 mutants of Arabidopsis. Plant Cell 2:1071–1080

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liscum E, Reed JW (2002) Genetics of Aux/IAA and ARF action in plant growth and development. Plant Mol Biol 49:387–400

    Article  CAS  PubMed  Google Scholar 

  • López-Arredondo DL, Leyva-González MA, González-Morales SI, López-Bucio J, Herrera-Estrella L (2014) Phosphate nutrition: improving low-phosphate tolerance in crops. Annu Rev Plant Biol 65:95–123

    Article  PubMed  Google Scholar 

  • López-Bucio J, Hernández-Abreu E, Sánchez-Calderón L, Nieto-Jacobo MF, Simpson J, Herrera-Estrella L (2002) Phosphorus availability alters root architecture and causes changes in hormone sensitivity in the Arabidopsis root system. Plant Physiol 129:244–256

    Article  PubMed  PubMed Central  Google Scholar 

  • López-Bucio J, Hernández-Madrigal F, Cervantes C, Ortiz-Castro R, Carreón-Abud Y, Martínez-Trujillo M (2014) Phosphate relieves chromium toxicity in Arabidopsis thaliana plants by interfering with chromate uptake. Biometals 27:363–370

    Article  PubMed  Google Scholar 

  • López-Bucio J, Ortiz-Castro R, Ruiz-Herrera LF, Vargas-Juárez C, 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 28:353–365

    Article  PubMed  Google Scholar 

  • MacGregor DR, Deak KI, Ingram PA, Malamy JE (2008) Root system architecture in Arabidopsis grown in culture is regulated by sucrose uptake in the aerial tissues. The Plant Cell 20:2643–2660

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 signalling in Arabidopsis thaliana. Plant Mol Biol 86:35–50

    Article  PubMed  Google Scholar 

  • Michniewicz M, Brewer PB, Friml J (2007) Polar auxin transport and asymmetric auxin distribution open Access. The Arabidopsis Book 5:e0108. doi:10.1199/tab.0108 2007.

    PubMed  PubMed Central  Google Scholar 

  • Muday GK, DeLong A (2001) Polar auxin transport: controlling where and how much. Trends Plant Sci 6:535–542

    Article  CAS  PubMed  Google Scholar 

  • Muday GK, Rahman A, Binder BM (2012) Auxin and ethylene: collaborators or competitors? Trends Plant Sci 17:181–195

    Article  CAS  PubMed  Google Scholar 

  • Müller A, Guan C, Gälweiler L, Tänzler P, Huijser P, Marchant A, Parry G, Bennett M, Wisman E, Palme K (1998) AtPIN2 defines a locus of Arabidopsis for root gravitropism control. EMBO J 17:6903–6911

    Article  PubMed  PubMed Central  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Parry G, Calderon-Villalobos LI, Priggeb M, Peretc B, Dharmasiria S, Itohd H, Lechnera E, Grayd E, Bennett WM, Estelle M M (2009) Complex regulation of the TIR1/AFB family of auxin receptors. Proc Natl Acad Sci USA 106:22540–22545

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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, Perez-Amador MA, Yun J, Alonso J, Beemste TS, 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 24:2874–2885

    Article  PubMed  PubMed Central  Google Scholar 

  • Pickett FB, Wilson AK, Estelle M (1990) The aux1 mutation of Arabidopsis confers both auxin and ethylene resistance. Plant Physiol 94:1462–1466

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Potters G, Pasternak TP, Guisez Y, Palme KJ, Jansen AK (2007) Stress-induced morphogenic responses: growing out of trouble? Trends Plant Sci 12:98–105

    Article  CAS  PubMed  Google Scholar 

  • Ruan YL (2014) Sucrose metabolism: gateway to diverse carbon use and sugar signalling. Annu Rev Plant Biol 65:33–67

    Article  CAS  PubMed  Google Scholar 

  • 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 99:463–472

    Article  CAS  PubMed  Google Scholar 

  • Sánchez-Calderón L, López-Bucio J, Chacón-López A, Cruz-Ramírez A, Nieto-Jacobo F, Dubrovsky JG, Herrera-Estrella L (2005) Phosphate starvation induces a determinate developmental program in the roots of Arabidopsis thaliana. Plant Cell Physiol 46:174–178

    Article  PubMed  Google Scholar 

  • Shanker AK, Cervantes C, Loza-Tavera H, Avudainayagam S (2005) Chromium toxicity in plants. Environ Int 31:739–775

    Article  CAS  PubMed  Google Scholar 

  • Shupack SI (1991) The chemistry of chromium and some resulting analytical problems. Environ Health Perspect 92:7–11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stohs SJ, Bagchi D (1995) Mechanisms in the toxicity of metal ions. Free Radical Biol Med 18:321–336

    Article  CAS  Google Scholar 

  • Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin elements. Plant Cell 7:288–299

    Google Scholar 

  • Xiong Y, Sheen J (2012) Rapamycin and glucose-target of rapamycin (TOR) protein signalling in plants. J Biol Chem 287:2836–2842

    Article  CAS  PubMed  Google Scholar 

  • Xiong Y, McCormack M, Li L, Hall Q, Xiang C, Sheen Jen J (2013) Glc-TOR signalling leads transcriptome reprogramming and meristem activation. Nature 496:181–186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang L, Xu M, Koo Y, He J, Poethig RS (2013) Sugar promotes vegetative phase change in Arabidopsis thaliana by repressing the expression of MIR156A and MIR156C. eLife 2:e00260. doi:10.7554/eLife.00260

    PubMed  PubMed Central  Google Scholar 

  • Yu S, Cao L, Zhou CM, Zhang TQ, Lian H, Sun Y, Wu J, Huang J, Wang G, Wang JW (2013) Sugar is an endogenous cue for juvenile-to-adult phase transition in plants. eLife 2:e00269. doi:10.7554/eLife.00269

    PubMed  PubMed Central  Google Scholar 

  • Zakhartsev M, Medvedeva I, Orlov Y, Akberdin I, Krebs O, Schulze WX (2016) Metabolic model of central carbon and energy metabolisms of growing Arabidopsis thaliana in relation to sucrose translocation. BMC Plant Biol 16:262. doi: 10.1186/s12870-016-0868-3

    Article  PubMed  PubMed Central  Google Scholar 

  • Zimmermann P, Hirsch-Hoffman M, Hennig L, Gruissem W (2004) GENEVESTIGATOR: Arabidopsis microarray database and analysis toolbox. Plant Physiol 136:2621–2632

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Drs. Mark A. Estelle and Alfredo Cruz-Ramírez are thanked for providing us Arabidopsis mutant and transgenic lines. This work was supported by grants from the Consejo Nacional de Ciencia y Tecnología (CONACYT, México, Grant Nos. 177775, and 169769), and the Consejo de la Investigación Científica (UMSNH, México, Grant No. CIC 2.26).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to José López-Bucio or Miguel Martínez-Trujillo.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hernández-Madrigal, F., Ortiz-Castro, R., Ruiz-Herrera, L.F. et al. Sucrose Protects Arabidopsis Roots from Chromium Toxicity Influencing the Auxin–Plethora Signaling Pathway and Improving Meristematic Cell Activity. J Plant Growth Regul 37, 530–538 (2018). https://doi.org/10.1007/s00344-017-9751-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-017-9751-1

Keywords

Navigation