Enhanced proton translocating pyrophosphatase activity improves nitrogen use efficiency in romaine lettuce

Julio Paez-Valencia, Jonathan Sanchez-Lares, Ellen Marsh, Liane T. Dorneles, Mirella P. Santos, Diego Sanchez, Alexander Winter, Sean Murphy, Jennifer Cox, Marcin Trzaska, Jason Metler, Alex Kozic, Arnoldo R. Facanha, Daniel Schachtman, Charles A Sanchez, Roberto A. Gaxiola

Research output: Contribution to journalArticle

37 Citations (Scopus)

Abstract

Plant nitrate (NO3-) acquisition depends on the combined activities of root high- and low-affinity NO3- transporters and the proton gradient generated by the plasma membrane H+-ATPase. These processes are coordinated with photosynthesis and the carbon status of the plant. Here, we present the characterization of romaine lettuce (Lactuca sativa 'Conquistador') plants engineered to overexpress an intragenic gain-of-function allele of the type I proton translocating pyrophosphatase (H+-PPase) of Arabidopsis (Arabidopsis thaliana). The proton-pumping and inorganic pyrophosphate hydrolytic activities of these plants are augmented compared with control plants. Immunohistochemical data show a conspicuous increase in H+-PPase protein abundance at the vasculature of the transgenic plants. Transgenic plants displayed an enhanced rhizosphere acidification capacity consistent with the augmented plasma membrane H+-ATPase proton transport values, and ATP hydrolytic capacities evaluated in vitro. These transgenic lines outperform control plants when challenged with NO3- limitations in laboratory, greenhouse, and field scenarios. Furthermore, we report the characterization of a lettuce LsNRT2.1 gene that is constitutive up-regulated in the transgenic plants. Of note, the expression of the LsNRT2.1 gene in control plants is regulated by NO3- and sugars. Enhanced accumulation of 15N-labeled fertilizer by transgenic lettuce compared with control plants was observed in greenhouse experiments. A negative correlation between the level of root soluble sugars and biomass is consistent with the strong root growth that characterizes these transgenic plants.

Original languageEnglish (US)
Pages (from-to)1557-1569
Number of pages13
JournalPlant Physiology
Volume161
Issue number3
DOIs
StatePublished - 2013

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Inorganic Pyrophosphatase
romaine lettuce
pyrophosphatases
Lettuce
nutrient use efficiency
protons
Nitrogen
Genetically Modified Plants
transgenic plants
Protons
H-transporting ATP synthase
Proton-Translocating ATPases
Arabidopsis
lettuce
plasma membrane
Cell Membrane
genetically modified organisms
sugars
Rhizosphere
pyrophosphates

ASJC Scopus subject areas

  • Plant Science
  • Genetics
  • Physiology

Cite this

Paez-Valencia, J., Sanchez-Lares, J., Marsh, E., Dorneles, L. T., Santos, M. P., Sanchez, D., ... Gaxiola, R. A. (2013). Enhanced proton translocating pyrophosphatase activity improves nitrogen use efficiency in romaine lettuce. Plant Physiology, 161(3), 1557-1569. https://doi.org/10.1104/pp.112.212852

Enhanced proton translocating pyrophosphatase activity improves nitrogen use efficiency in romaine lettuce. / Paez-Valencia, Julio; Sanchez-Lares, Jonathan; Marsh, Ellen; Dorneles, Liane T.; Santos, Mirella P.; Sanchez, Diego; Winter, Alexander; Murphy, Sean; Cox, Jennifer; Trzaska, Marcin; Metler, Jason; Kozic, Alex; Facanha, Arnoldo R.; Schachtman, Daniel; Sanchez, Charles A; Gaxiola, Roberto A.

In: Plant Physiology, Vol. 161, No. 3, 2013, p. 1557-1569.

Research output: Contribution to journalArticle

Paez-Valencia, J, Sanchez-Lares, J, Marsh, E, Dorneles, LT, Santos, MP, Sanchez, D, Winter, A, Murphy, S, Cox, J, Trzaska, M, Metler, J, Kozic, A, Facanha, AR, Schachtman, D, Sanchez, CA & Gaxiola, RA 2013, 'Enhanced proton translocating pyrophosphatase activity improves nitrogen use efficiency in romaine lettuce', Plant Physiology, vol. 161, no. 3, pp. 1557-1569. https://doi.org/10.1104/pp.112.212852
Paez-Valencia J, Sanchez-Lares J, Marsh E, Dorneles LT, Santos MP, Sanchez D et al. Enhanced proton translocating pyrophosphatase activity improves nitrogen use efficiency in romaine lettuce. Plant Physiology. 2013;161(3):1557-1569. https://doi.org/10.1104/pp.112.212852
Paez-Valencia, Julio ; Sanchez-Lares, Jonathan ; Marsh, Ellen ; Dorneles, Liane T. ; Santos, Mirella P. ; Sanchez, Diego ; Winter, Alexander ; Murphy, Sean ; Cox, Jennifer ; Trzaska, Marcin ; Metler, Jason ; Kozic, Alex ; Facanha, Arnoldo R. ; Schachtman, Daniel ; Sanchez, Charles A ; Gaxiola, Roberto A. / Enhanced proton translocating pyrophosphatase activity improves nitrogen use efficiency in romaine lettuce. In: Plant Physiology. 2013 ; Vol. 161, No. 3. pp. 1557-1569.
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AU - Winter, Alexander

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