pp 1–13 | Cite as

Mitogen-activated protein kinase 6 integrates phosphate and iron responses for indeterminate root growth in Arabidopsis thaliana

  • Jesús Salvador López-BucioEmail author
  • Guadalupe Jessica Salmerón-Barrera
  • Gustavo Ravelo-Ortega
  • Javier Raya-González
  • Patricia León
  • Homero Reyes de la Cruz
  • Jesús Campos-García
  • José López-Bucio
  • Ángel Arturo Guevara-GarcíaEmail author
Original Article


Main conclusion

A MAPK module, of which MPK6 kinase is an important component, is involved in the coordination of the responses to Pi and Fe in the primary root meristem of Arabidopsis thaliana.


Phosphate (Pi) deficiency induces determinate primary root growth in Arabidopsis through cessation of cell division in the meristem, which is linked to an increased iron (Fe) accumulation. Here, we show that Mitogen-Activated Protein Kinase6 (MPK6) has a role in Arabidopsis primary root growth under low Pi stress. MPK6 activity is induced in roots in response to low Pi, and such induction is enhanced by Fe supplementation, suggesting an MPK6 role in coordinating Pi/Fe balance in mediating root growth. The differentiation of the root meristem induced by low Pi levels correlates with altered expression of auxin-inducible genes and auxin transporter levels via MPK6. Our results indicate a critical role of the MPK6 kinase in coordinating meristem cell activity to Pi and Fe availability for proper primary root growth.


Low Pi stress MAPK6 Phosphate/iron balance Root development 



Synthetic auxin-response element


Green fluorescent protein


Mitogen-activated protein kinase


Mitogen-activated protein kinase 3 and 6


PIN-formed efflux auxin transporters 1 and 2


Root apical meristem



We thank Dr. León Francisco Ruíz-Herrera by his technical support for confocal microscopic analysis. This work was supported by grants from the Consejo Nacional de Ciencia y Tecnología (CONACYT, México, 177775 to JLB, 251848 to AAGG and cátedra CONACYT No. 416 to JSLB), the Consejo de la Investigación Científica (UMSNH, México, grant no. CIC 2.26), and the UNAM-DGAPA-PAPIIT (Grants IN207014 and IN210917 to AAGG and JSLB and IN204617 to PL).

Supplementary material

425_2019_3212_MOESM1_ESM.pdf (32.9 mb)
Supplementary file 1 33700kb


  1. Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, Gomez-Gomez L, Boller T, Ausubel FM, Sheen J (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415(6875):977–983. Google Scholar
  2. Balzergue C, Dartevelle T, Godon C, Laugier E, Meisrimler C, Teulon JM, Creff A, Bissler M, Brouchoud C, Hagège A et al (2017) Low phosphate activates STOP1-ALMT1 to rapidly inhibit root cell elongation. Nat Commun 8:15300Google Scholar
  3. Bates TR, Lynch JP (1996) Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability. Plant Cell Environ 19:529–538Google Scholar
  4. Belal R, Tang R, Li Y, Mabrouk Y, Badr E, Luan S (2015) An ABC transporter complex encoded by Aluminum Sensitive 3 and NAP3 is required for phosphate deficiency responses in Arabidopsis. Biochem Biophys Res Commun 463(2):18–23. Google Scholar
  5. Benková E, Michniewicz M, Sauer M, Teichmann T, Seifertova D, Jurgens G, Friml J (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115(5):591–602Google Scholar
  6. 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(7021):39–44. Google Scholar
  7. Bush SM, Krysan PJ (2007) Mutational evidence that the Arabidopsis MAP kinase MPK6 is involved in anther, inflorescence, and embryo development. J Exp Bot 58(8):2181–2191. Google Scholar
  8. Contreras-Cornejo HA, Lopez-Bucio JS, Mendez-Bravo A, Macias-Rodriguez L, Ramos-Vega M, Guevara-Garcia AA, Lopez-Bucio J (2015) Mitogen-activated protein kinase 6 and ethylene and auxin signaling pathways are involved in Arabidopsis root-system architecture alterations by Trichoderma atroviride. Mol Plant Microbe Interact 28(6):701–710. Google Scholar
  9. Devaiah BN, Karthikeyan AS, Raghothama KG (2007) WRKY75 transcription factor is a modulator of phosphate acquisition and root development in Arabidopsis. Plant Physiol 143(4):1789–1801. Google Scholar
  10. Dolan L, Janmaat K, Willemsen V, Linstead P, Poethig S, Roberts K, Scheres B (1993) Cellular organisation of the Arabidopsis thaliana root. Development 119(1):71–84Google Scholar
  11. Dong J, Piñeros MA, Li X, Yang H, Liu Y, Murphy AS, Kochian LV, Liu D (2017) An Arabidopsis ABC transporter mediates phosphate deficiency-induced remodeling of root architecture by modulating iron homeostasis in roots. Molecular Plant 10(2):244–259. Google Scholar
  12. Giehl RF, von Wiren N (2014) Root nutrient foraging. Plant Physiol 166(2):509–517. Google Scholar
  13. Gutiérrez-Alanís D, Yong-Villalobos L, Jiménez-Sandoval P, Alatorre-Cobos F, Oropeza-Aburto A, Mora-Macías J, Sánchez-Rodríguez F, Cruz-Ramírez A, Herrera-Estrella L (2017) Phosphate starvation dependent iron mobilization induces CLE14 expression to trigger root meristem differentiation through CLV2/PEPR2 signaling. Dev Cell 41:555–570.e3Google Scholar
  14. Hamel LP, Nicole MC, Sritubtim S, Morency MJ, Ellis M, Ehlting J, Beaudoin N, Barbazuk B, Klessig D, Lee J, Martin G, Mundy J, Ohashi Y, Scheel D, Sheen J, Xing T, Zhang S, Seguin A, Ellis BE (2006) Ancient signals: comparative genomics of plant MAPK and MAPKK gene families. Trends Plant Sci 11(4):192–198. Google Scholar
  15. Hirsch J, Marin E, Floriani M, Chiarenza S, Richaud P, Nussaume L, Thibaud MC (2006) Phosphate deficiency promotes modification of iron distribution in Arabidopsis plants. Biochimie 88(11):1767–1771. Google Scholar
  16. Hoehenwarter W, Monchgesang S, Neumann S, Majovsky P, Abel S, Muller J (2016) Comparative expression profiling reveals a role of the root apoplast in local phosphate response. BMC Plant Biol 16:106. Google Scholar
  17. Jonak C, Nakagami H, Hirt H (2004) Heavy metal stress. Activation of distinct mitogen-activated protein kinase pathways by copper and cadmium. Plant Physiol 136(2):3276–3283. Google Scholar
  18. Kong X, Liu G, Liu J, Ding Z (2018) The root transition zone: a hot spot for signal crosstalk. Trends Plant Sci 23(5):403–409. Google Scholar
  19. Larsen PB, Geisler MJB, Jones CA, Williams KM, Cancel JD (2005) ALS3 encodes a phloem-localized ABC transporter-like protein that is required for aluminum tolerance in Arabidopsis. Plant J 41(3):353–363. Google Scholar
  20. Lei L, Li Y, Wang Q, Xu J, Chen Y, Yang H, Ren D (2014) Activation of MKK9-MPK3/MPK6 enhances phosphate acquisition in Arabidopsis thaliana. New Phytol 203(4):1146–1160. Google Scholar
  21. Leyser O (2010) The power of auxin in plants. Plant Physiol 154(2):501–505. Google Scholar
  22. Liu Y, Zhang S (2004) Phosphorylation of 1-aminocyclopropane-1-carboxylic acid synthase by MPK6, a stress-responsive mitogen-activated protein kinase, induces ethylene biosynthesis in Arabidopsis. Plant Cell 16(12):3386–3399. Google Scholar
  23. Liu XM, Kim KE, Kim KC, Nguyen XC, Han HJ, Jung MS, Kim HS, Kim SH, Park HC, Yun DJ, Chung WS (2010) Cadmium activates Arabidopsis MPK3 and MPK6 via accumulation of reactive oxygen species. Phytochemistry 71(5–6):614–618. Google Scholar
  24. López-Bucio J, Hernández-Abreu E, Sánchez-Cálderon L, Nieto-Jacobo MF, Simpson J, Herrera-Estrella L (2002) Phosphate availability alters architecture and causes changes in hormone sensitivity in the Arabidopsis root system. Plant Physiol 129(1):244–256. Google Scholar
  25. López-Bucio J, Cruz-Ramírez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol 6(3):280–287Google Scholar
  26. López-Bucio J, Hernández-Madrigal F, Cervantes C, Ortiz-Castro R, Carreon-Abud Y, Martínez-Trujillo M (2014a) Phosphate relieves chromium toxicity in Arabidopsis thaliana plants by interfering with chromate uptake. Biometals 27(2):363–370. Google Scholar
  27. López-Bucio JS, Dubrovsky JG, Raya-Gonzalez J, Ugartechea-Chirino Y, López-Bucio J, de Luna-Valdez LA, Ramos-Vega M, Leon P, Guevara-Garcia AA (2014b) Arabidopsis thaliana mitogen-activated protein kinase 6 is involved in seed formation and modulation of primary and lateral root development. J Exp Bot 65(1):169–183. Google Scholar
  28. López-Bucio JS, Raya-Gonzalez J, Ravelo-Ortega G, Ruíz-Herrera LF, Ramos-Vega M, León P, López-Bucio J, Guevara-García AA (2018) Mitogen activated protein kinase 6 and map kinase phosphatase 1 are involved in the response of Arabidopsis roots to L-glutamate. Plant Mol Biol 96:339–351. Google Scholar
  29. Lu C, Han MH, Guevara-García A, Fedoroff NV (2002) Mitogen-activated protein kinase signaling in postgermination arrest of development by abscisic acid. Proc Natl Acad Sci USA 99(24):15812–15817. Google Scholar
  30. Meng X, Wang H, He Y, Liu Y, Walker JC, Torii KU, Zhang S (2012) A MAPK cascade downstream of ERECTA receptor-like protein kinase regulates Arabidopsis inflorescence architecture by promoting localized cell proliferation. Plant Cell 24(12):4948–4960. Google Scholar
  31. Mishra NS, Tuteja R, Tuteja N (2006) Signaling through MAP kinase networks in plants. Arch Biochem Biophys 452(1):55–68. Google Scholar
  32. Mora-Macías J, Ojeda-Rivera JO, Gutiérrez-Alanís D, Yong-Villalobos L, Oropeza-Aburto A, Raya-González J, Jiménez-Domínguez G, Chávez-Calvillo G, Rellán-Álvarez R, Herrera-Estrella L (2017) Malate-dependent Fe accumulation is a critical checkpoint in the root developmental response to low phosphate. Proc Natl Acad Sci USA 114:E3563–E3572Google Scholar
  33. Müller M, Schmidt W (2004) Environmentally induced plasticity of root hair development in Arabidopsis. Plant Physiol 134:409–419Google Scholar
  34. Müller J, Toev T, Heisters M, Teller J, Moore KL, Hause G, Dinesh DC, Burstenbinder K, Abel S (2015) Iron-dependent callose deposition adjusts root meristem maintenance to phosphate availability. Dev Cell 33(2):216–230. Google Scholar
  35. 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(5):2987–2991. Google Scholar
  36. Pérez-Torres CA, López-Bucio J, Cruz-Ramírez A, Ibarra-Laclette E, Dharmasiri S, Estelle M, Herrera-Estrella L (2008) Phosphate availability alters lateral root development in Arabidopsis by modulating auxin sensitivity via a mechanism involving the TIR1 auxin receptor. Plant Cell 20(12):3258–3272. Google Scholar
  37. Popescu SC, Popescu GV, Bachan S, Zhang Z, Gerstein M, Snyder M, Dinesh-Kumar SP (2009) MAPK target networks in Arabidopsis thaliana revealed using functional protein microarrays. Genes Dev 23(1):80–92. Google Scholar
  38. Rai V, Sanagala R, Sinilal B, Yadav S, Sarkar AK, Dantu PK, Jain A (2015) Iron availability affects phosphate deficiency-mediated responses, and evidence of cross-talk with auxin and zinc in Arabidopsis. Plant Cell Physiol 56(6):1107–1123. Google Scholar
  39. Roschzttardtz H, Conéjéro G, Curie C, Mari S (2009) Identification of the endodermal vacuole as the iron storage compartment in the Arabidopsis embryo. Plant Physiol 151(3):1329–1338. Google Scholar
  40. Ruiz Herrera LF, Shane MW, López-Bucio J (2015) Nutritional regulation of root development. Wiley Interdiscip Rev Dev Biol 4(4):431–443. Google Scholar
  41. Sánchez-Calderón L, López-Bucio J, Chacon-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(1):174–184. Google Scholar
  42. Stadler R, Brandner J, Schulz A, Gahrtz M, Sauer N (1995) Phloem loading by the PmSUC2 sucrose carrier from Plantago major occurs into companion cells. Plant Cell 7(10):1545–1554. Google Scholar
  43. Svistoonoff S, Creff A, Reymond M, Sigoillot-Claude C, Ricaud L, Blanchet A, Nussaume L, Desnos T (2007) Root tip contact with low-phosphate media reprograms plant root architecture. Nat Genet 39(6):792–796. Google Scholar
  44. Takahashi F, Yoshida R, Ichimura K, Mizoguchi T, Seo S, Yonezawa M, Maruyama K, Yamaguchi-Shinozaki K, Shinozaki K (2007) The mitogen-activated protein kinase cascade MKK3-MPK6 is an important part of the jasmonate signal transduction pathway in Arabidopsis. Plant Cell 19(3):805–818. Google Scholar
  45. Ticconi CA, Lucero RD, Sakhonwasee S, Adamson AW, Creff A, Nussaume L, Desnos T, Abel S (2009) ER-resident proteins PDR2 and LPR1 mediate the developmental response of root meristems to phosphate availability. Proc Natl Acad Sci USA 106(33):14174–14179. Google Scholar
  46. Tokizawa M, Kobayashi Y, Saito T, Kobayashi M, Iuchi S, Nomoto M, Tada Y, Yamamoto YY, Koyama H (2015) Sensitive to Proton Rhizotoxicity1, Calmodulin Binding Transcription Activator2, and other transcription factors are involved in Aluminum-Activated Malate Transporter1 expression. Plant Physiol 167(3):991–1003. Google Scholar
  47. Ulm R, Ichimura K, Mizoguchi T, Peck SC, Zhu T, Wang X, Shinozaki K, Paszkowski J (2002) Distinct regulation of salinity and genotoxic stress responses by Arabidopsis MAP kinase phosphatase 1. EMBO J 21(23):6483–6493Google Scholar
  48. Vieten A, Vanneste S, Wisniewska J, Benkova E, Benjamins R, Beeckman T, Luschnig C, Friml J (2005) Functional redundancy of PIN proteins is accompanied by auxin-dependent cross-regulation of PIN expression. Development 132(20):4521–4531. Google Scholar
  49. Wang H, Ngwenyama N, Liu Y, Walker JC, Zhang S (2007) Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis. Plant Cell 19(1):63–73. Google Scholar
  50. Wang P, Du Y, Li Y, Ren D, Song CP (2010) Hydrogen peroxide-mediated activation of MAP kinase 6 modulates nitric oxide biosynthesis and signal transduction in Arabidopsis. Plant Cell 22(9):2981–2998. Google Scholar
  51. Wang X, Wang Z, Zheng Z, Dong J, Song L, Sui L, Nussaume L, Desnos T, Liu D (2019) Genetic dissection of Fe-dependent signaling in root developmental responses to phosphate deficiency. Plant Physiol 179(1):300–316. Google Scholar
  52. Ward JT, Lahner B, Yakubova E, Salt DE, Raghothama KG (2008) The effect of iron on the primary root elongation of Arabidopsis during phosphate deficiency. Plant Physiol 147(3):1181–1191. Google Scholar
  53. Xu J, Xie J, Yan C, Zou X, Ren D, Zhang S (2014) A chemical genetic approach demonstrates that MPK3/MPK6 activation and NADPH oxidase-mediated oxidative burst are two independent signaling events in plant immunity. Plant J 77(2):222–234. Google Scholar
  54. Yan JY, Li CX, Sun L, Ren JY, Li GX, Ding ZJ, Zheng SJ (2016) A WRKY transcription factor regulates Fe translocation under Fe deficiency. Plant Physiol 171(3):2017–2027. Google Scholar
  55. Yoo SD, Cho YH, Tena G, Xiong Y, Sheen J (2008) Dual control of nuclear EIN3 by bifurcate MAPK cascades in C2H4 signalling. Nature 451(7180):789–795. Google Scholar
  56. Zheng H, Pan X, Deng Y, Wu H, Liu P, Li X (2016) AtOPR3 specifically inhibits primary root growth in Arabidopsis under phosphate deficiency. Sci Rep 6:24778. Google Scholar

Copyright information

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

Authors and Affiliations

  • Jesús Salvador López-Bucio
    • 1
    Email author
  • Guadalupe Jessica Salmerón-Barrera
    • 2
  • Gustavo Ravelo-Ortega
    • 2
  • Javier Raya-González
    • 2
  • Patricia León
    • 3
  • Homero Reyes de la Cruz
    • 2
  • Jesús Campos-García
    • 2
  • José López-Bucio
    • 2
  • Ángel Arturo Guevara-García
    • 3
    Email author
  1. 1.CONACYT-Instituto de Investigaciones Químico BiológicasUniversidad Michoacana de San Nicolás de HidalgoMoreliaMexico
  2. 2.Instituto de Investigaciones Químico BiológicasUniversidad Michoacana de San Nicolás de HidalgoMoreliaMexico
  3. 3.Instituto de BiotecnologíaUniversidad Nacional Autónoma de MéxicoCuernavacaMexico

Personalised recommendations