Constitutive and companion cell-specific overexpression of AVP1, encoding a proton-pumping pyrophosphatase, enhances biomass accumulation, phloem loading, and long-distance transport1[OPEN]

Aswad S. Khadilkar, Umesh P. Yadav, Carolina Salazar, Vladimir Shulaev, Julio Paez-Valencia, Gaston A. Pizzio, Roberto Gaxiola, Brian G. Ayre

Research output: Contribution to journalArticle

34 Scopus citations

Abstract

Plant productivity is determined in large part by the partitioning of assimilates between the sites of production and the sites of utilization. Proton-pumping pyrophosphatases (H+-PPases) are shown to participate in many energetic plant processes, including general growth and biomass accumulation, CO2 fixation, nutrient acquisition, and stress responses. H+-PPases have a well-documented role in hydrolyzing pyrophosphate (PPi) and capturing the released energy to pump H+ across the tonoplast and endomembranes to create proton motive force (pmf). Recently, an additional role for H+-PPases in phloem loading and biomass partitioning was proposed. In companion cells (CCs) of the phloem, H+-PPases localize to the plasma membrane rather than endomembranes, and rather than hydrolyzing PPi to create pmf, pmf is utilized to synthesize PPi. Additional PPi in the CCs promotes sucrose oxidation and ATP synthesis, which the plasma membrane P-type ATPase in turn uses to create more pmf for phloem loading of sucrose via sucrose-H+ symporters. To test this model, transgenic Arabidopsis (Arabidopsis thaliana) plants were generated with constitutive and CC-specific overexpression of AVP1, encoding type 1 ARABIDOPSIS VACUOLAR PYROPHOSPHATASE1. Plants with both constitutive and CC-specific overexpression accumulated more biomass in shoot and root systems. 14C-labeling experiments showed enhanced photosynthesis, phloem loading, phloem transport, and delivery to sink organs. The results obtained with constitutive and CC-specific promoters were very similar, such that the growth enhancement mediated by AVP1 overexpression can be attributed to its role in phloem CCs. This supports the model for H+-PPases functioning as PPi synthases in the phloem by arguing that the increases in biomass observed with AVP1 overexpression stem from improved phloem loading and transport.

Original languageEnglish (US)
Pages (from-to)401-414
Number of pages14
JournalPlant Physiology
Volume170
Issue number1
DOIs
StatePublished - Jan 2016

ASJC Scopus subject areas

  • Physiology
  • Genetics
  • Plant Science

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