Arabidopsis Type I Proton-Pumping Pyrophosphatase Expresses Strongly in Phloem, Where It Is Required for Pyrophosphate Metabolism and Photosynthate Partitioning

• Published in: Plant physiology (Bethesda) 2015-04, Vol.167 (4), p.1541-1553
• Main Authors: Pizzio, Gaston A., Paez-Valencia, Julio, Khadilkar, Aswad S., Regmi, Kamesh, Patron-Soberano, Araceli, Zhang, Shangji, Sanchez-Lares, Jonathan, Furstenau, Tara, Li, Jisheng, Sanchez-Gomez, Concepcion, Valencia-Mayoral, Pedro, Yadav, Umesh P., Ayre, Brian G., Gaxiola, Roberto A.
• Format: Article
• Language: English
• Subjects: American culture; Arabidopsis - enzymology; Arabidopsis - genetics; Arabidopsis - growth & development; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Diphosphates - metabolism; Gene Expression; Gene Expression Regulation, Plant; Genes, Reporter; Homeostasis; Inorganic Pyrophosphatase - genetics; Inorganic Pyrophosphatase - metabolism; Leaves; MEMBRANES, TRANSPORT, AND BIOENERGETICS; Mutation; Organ Specificity; Phenotype; Phenotypes; Phloem; Phloem - enzymology; Phloem - genetics; Phloem loading; Plant growth; Plant Leaves - enzymology; Plant Leaves - genetics; Plant Leaves - growth & development; Plant roots; Plant Roots - enzymology; Plant Roots - genetics; Plant Roots - growth & development; Plant Shoots - enzymology; Plant Shoots - genetics; Plant Shoots - growth & development; Plants; Plants, Genetically Modified; Promoter Regions, Genetic - genetics; Seedlings; Seedlings - enzymology; Seedlings - genetics; Seedlings - growth & development; Sucrose - metabolism; Transgenic plants
• ISSN: 0032-0889; 1532-2548
• DOI: 10.1104/pp.114.254342

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 transcriptionalAVP1promoter:: GUS fusion revealed phloem activity in source leaves. UbiquitousAVP1overexpression (35S::AVP1cassette) 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, andPHOSPHATE TRANSPORTER1.4[PHT1.4]). Phloem-specificAVP1overexpression (Commelina Yellow Mottle Virus promoter[pCOYMV]::AVP1) elicited similar phenotypes. By contrast, phloem-specificAVP1knockdown (pCoYMV:: RNAiAVP1)resulted in stunted seedlings in sucrose-deprived medium. We also present a promoter mutantavp1-2(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 anEscherichia colisoluble pyrophosphatase in the phloem (pCoYMV::pyrophosphatase) ofavp1-2plants 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.