Arabidopsis type i proton-pumping pyrophosphatase expresses strongly in phloem, where it is required for pyrophosphate metabolism and photosynthate partitioning

Gaston A. Pizzio, Julio Paez-Valencia, Aswad S. Khadilkar, Kamesh Regmi, Araceli Patron-Soberano, Shangji Zhang, Jonathan Sanchez-Lares, Tara Furstenau, Jisheng Li, Concepcion Sanchez-Gomez, Pedro Valencia-Mayoral, Umesh P. Yadav, Brian G. Ayre, Roberto Gaxiola

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40 Scopus citations

Abstract

Phloem loading is a critical process in plant physiology. The potential of regulating the translocation of photoassimilates from source to sink tissues represents an opportunity to increase crop yield. Pyrophosphate homeostasis is crucial for normal phloem function in apoplasmic loaders. The involvement of Arabidopsis (Arabidopsis thaliana) type I proton-pumping pyrophosphatase (AVP1) in phloem loading was analyzed at genetic, histochemical, and physiological levels. A transcriptional AVP1 promoter:: GUS fusion revealed phloem activity in source leaves. Ubiquitous AVP1 overexpression (35S::AVP1 cassette) enhanced shoot biomass, photoassimilate production and transport, rhizosphere acidification, and expression of sugar-induced root ion transporter genes (POTASSIUM TRANSPORTER2 [KUP2], NITRATE TRANSPORTER2.1 [NRT2.1], NRT2.4, and PHOSPHATE TRANSPORTER1.4 [PHT1.4]). Phloem-specific AVP1 overexpression (Commelina Yellow Mottle Virus promoter [pCOYMV]::AVP1) elicited similar phenotypes. By contrast, phloem-specific AVP1 knockdown (pCoYMV::RNAiAVP1) resulted in stunted seedlings in sucrose-deprived medium. We also present a promoter mutant avp1-2 (SALK046492) with a 70% reduction of expression that did not show severe growth impairment. Interestingly, AVP1 protein in this mutant is prominent in the phloem.Moreover, expression of an Escherichia colisoluble pyrophosphatase in the phloem (pCoYMV::pyrophosphatase) of avp1-2 plants resulted in severe dwarf phenotype and abnormal leaf morphology. We conclude that the Proton-Pumping Pyrophosphatase AVP1 localized at the plasma membrane of the sieve element-companion cell complexes functions as a synthase, and that this activity is critical for the maintenance of pyrophosphate homeostasis required for phloem function.

Original languageEnglish (US)
Pages (from-to)1541-1553
Number of pages13
JournalPlant Physiology
Volume167
Issue number4
DOIs
StatePublished - Apr 1 2015

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ASJC Scopus subject areas

  • Physiology
  • Genetics
  • Plant Science

Cite this

Pizzio, G. A., Paez-Valencia, J., Khadilkar, A. S., Regmi, K., Patron-Soberano, A., Zhang, S., Sanchez-Lares, J., Furstenau, T., Li, J., Sanchez-Gomez, C., Valencia-Mayoral, P., Yadav, U. P., Ayre, B. G., & Gaxiola, R. (2015). Arabidopsis type i proton-pumping pyrophosphatase expresses strongly in phloem, where it is required for pyrophosphate metabolism and photosynthate partitioning. Plant Physiology, 167(4), 1541-1553. https://doi.org/10.1104/pp.114.254342