The role of alanine synthesis and nitrate-induced nitric oxide production during hypoxia stress in Cucurbita pepo nectaries

Erik M. Solhaug; Rahul Roy; Rodney T. Venterea; Clay J. Carter

doi:10.1111/tpj.15055

The role of alanine synthesis and nitrate-induced nitric oxide production during hypoxia stress in Cucurbita pepo nectaries

Erik M. Solhaug, Rahul Roy, Rodney T. Venterea, Clay J. Carter

Plant and Microbial Biology

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5 Scopus citations

Abstract

Floral nectar is a sugary solution produced by nectaries to attract and reward pollinators. Nectar metabolites, such as sugars, are synthesized within the nectary during secretion from both pre-stored and direct phloem-derived precursors. In addition to sugars, nectars contain nitrogenous compounds such as amino acids; however, little is known about the role(s) of nitrogen (N) compounds in nectary function. In this study, we investigated N metabolism in Cucurbita pepo (squash) floral nectaries in order to understand how various N-containing compounds are produced and determine the role of N metabolism in nectar secretion. The expression and activity of key enzymes involved in primary N assimilation, including nitrate reductase (NR) and alanine aminotransferase (AlaAT), were induced during secretion in C. pepo nectaries. Alanine (Ala) accumulated to about 35% of total amino acids in nectaries and nectar during peak secretion; however, alteration of vascular nitrate supply had no impact on Ala accumulation during secretion, suggesting that nectar(y) amino acids are produced by precursors other than nitrate. In addition, nitric oxide (NO) is produced from nitrate and nitrite, at least partially by NR, in nectaries and nectar. Hypoxia-related processes are induced in nectaries during secretion, including lactic acid and ethanolic fermentation. Finally, treatments that alter nitrate supply affect levels of hypoxic metabolites, nectar volume and nectar sugar composition. The induction of N metabolism in C. pepo nectaries thus plays an important role in the synthesis and secretion of nectar sugar.

Original language	English (US)
Pages (from-to)	580-599
Number of pages	20
Journal	Plant Journal
Volume	105
Issue number	3
DOIs	https://doi.org/10.1111/tpj.15055
State	Published - Feb 2021

Bibliographical note

Funding Information:
The authors thank Drs. Neil Olszewski, Adrian Hegeman and John Ward of the University of Minnesota for helpful comments on this work. We thank Dr. Francesco Licausi for kindly providing the :GFP‐GUS transgenic seeds. We also thank Dr. Bruce Witthuhn and the University of Minnesota Center for Mass Spectrometry and Proteomics for assistance with amino acid analyses. Funding: National Science Foundation – 1339246. pPCO2

Funding Information:
The authors thank Drs. Neil Olszewski, Adrian Hegeman and John Ward of the University of Minnesota for helpful comments on this work. We thank Dr. Francesco Licausi for kindly providing the pPCO2:GFP-GUS transgenic seeds. We also thank Dr. Bruce Witthuhn and the University of Minnesota Center for Mass Spectrometry and Proteomics for assistance with amino acid analyses. Funding: National Science Foundation ? 1339246.

Publisher Copyright:
© 2020 Society for Experimental Biology and John Wiley & Sons Ltd

Keywords

Cucurbita pepo
alanine
amino acids
hypoxia
metabolism
nectar
nectary
nitrate
nitric oxide
nitrogen

PubMed: MeSH publication types

Journal Article
Research Support, U.S. Gov't, Non-P.H.S.

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title = "The role of alanine synthesis and nitrate-induced nitric oxide production during hypoxia stress in Cucurbita pepo nectaries",

abstract = "Floral nectar is a sugary solution produced by nectaries to attract and reward pollinators. Nectar metabolites, such as sugars, are synthesized within the nectary during secretion from both pre-stored and direct phloem-derived precursors. In addition to sugars, nectars contain nitrogenous compounds such as amino acids; however, little is known about the role(s) of nitrogen (N) compounds in nectary function. In this study, we investigated N metabolism in Cucurbita pepo (squash) floral nectaries in order to understand how various N-containing compounds are produced and determine the role of N metabolism in nectar secretion. The expression and activity of key enzymes involved in primary N assimilation, including nitrate reductase (NR) and alanine aminotransferase (AlaAT), were induced during secretion in C. pepo nectaries. Alanine (Ala) accumulated to about 35% of total amino acids in nectaries and nectar during peak secretion; however, alteration of vascular nitrate supply had no impact on Ala accumulation during secretion, suggesting that nectar(y) amino acids are produced by precursors other than nitrate. In addition, nitric oxide (NO) is produced from nitrate and nitrite, at least partially by NR, in nectaries and nectar. Hypoxia-related processes are induced in nectaries during secretion, including lactic acid and ethanolic fermentation. Finally, treatments that alter nitrate supply affect levels of hypoxic metabolites, nectar volume and nectar sugar composition. The induction of N metabolism in C. pepo nectaries thus plays an important role in the synthesis and secretion of nectar sugar.",

keywords = "Cucurbita pepo, alanine, amino acids, hypoxia, metabolism, nectar, nectary, nitrate, nitric oxide, nitrogen",

author = "Solhaug, {Erik M.} and Rahul Roy and Venterea, {Rodney T.} and Carter, {Clay J.}",

note = "Funding Information: The authors thank Drs. Neil Olszewski, Adrian Hegeman and John Ward of the University of Minnesota for helpful comments on this work. We thank Dr. Francesco Licausi for kindly providing the :GFP‐GUS transgenic seeds. We also thank Dr. Bruce Witthuhn and the University of Minnesota Center for Mass Spectrometry and Proteomics for assistance with amino acid analyses. Funding: National Science Foundation – 1339246. pPCO2 Funding Information: The authors thank Drs. Neil Olszewski, Adrian Hegeman and John Ward of the University of Minnesota for helpful comments on this work. We thank Dr. Francesco Licausi for kindly providing the pPCO2:GFP-GUS transgenic seeds. We also thank Dr. Bruce Witthuhn and the University of Minnesota Center for Mass Spectrometry and Proteomics for assistance with amino acid analyses. Funding: National Science Foundation ? 1339246. Publisher Copyright: {\textcopyright} 2020 Society for Experimental Biology and John Wiley & Sons Ltd",

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AU - Roy, Rahul

AU - Venterea, Rodney T.

AU - Carter, Clay J.

N1 - Funding Information: The authors thank Drs. Neil Olszewski, Adrian Hegeman and John Ward of the University of Minnesota for helpful comments on this work. We thank Dr. Francesco Licausi for kindly providing the :GFP‐GUS transgenic seeds. We also thank Dr. Bruce Witthuhn and the University of Minnesota Center for Mass Spectrometry and Proteomics for assistance with amino acid analyses. Funding: National Science Foundation – 1339246. pPCO2 Funding Information: The authors thank Drs. Neil Olszewski, Adrian Hegeman and John Ward of the University of Minnesota for helpful comments on this work. We thank Dr. Francesco Licausi for kindly providing the pPCO2:GFP-GUS transgenic seeds. We also thank Dr. Bruce Witthuhn and the University of Minnesota Center for Mass Spectrometry and Proteomics for assistance with amino acid analyses. Funding: National Science Foundation ? 1339246. Publisher Copyright: © 2020 Society for Experimental Biology and John Wiley & Sons Ltd

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N2 - Floral nectar is a sugary solution produced by nectaries to attract and reward pollinators. Nectar metabolites, such as sugars, are synthesized within the nectary during secretion from both pre-stored and direct phloem-derived precursors. In addition to sugars, nectars contain nitrogenous compounds such as amino acids; however, little is known about the role(s) of nitrogen (N) compounds in nectary function. In this study, we investigated N metabolism in Cucurbita pepo (squash) floral nectaries in order to understand how various N-containing compounds are produced and determine the role of N metabolism in nectar secretion. The expression and activity of key enzymes involved in primary N assimilation, including nitrate reductase (NR) and alanine aminotransferase (AlaAT), were induced during secretion in C. pepo nectaries. Alanine (Ala) accumulated to about 35% of total amino acids in nectaries and nectar during peak secretion; however, alteration of vascular nitrate supply had no impact on Ala accumulation during secretion, suggesting that nectar(y) amino acids are produced by precursors other than nitrate. In addition, nitric oxide (NO) is produced from nitrate and nitrite, at least partially by NR, in nectaries and nectar. Hypoxia-related processes are induced in nectaries during secretion, including lactic acid and ethanolic fermentation. Finally, treatments that alter nitrate supply affect levels of hypoxic metabolites, nectar volume and nectar sugar composition. The induction of N metabolism in C. pepo nectaries thus plays an important role in the synthesis and secretion of nectar sugar.

AB - Floral nectar is a sugary solution produced by nectaries to attract and reward pollinators. Nectar metabolites, such as sugars, are synthesized within the nectary during secretion from both pre-stored and direct phloem-derived precursors. In addition to sugars, nectars contain nitrogenous compounds such as amino acids; however, little is known about the role(s) of nitrogen (N) compounds in nectary function. In this study, we investigated N metabolism in Cucurbita pepo (squash) floral nectaries in order to understand how various N-containing compounds are produced and determine the role of N metabolism in nectar secretion. The expression and activity of key enzymes involved in primary N assimilation, including nitrate reductase (NR) and alanine aminotransferase (AlaAT), were induced during secretion in C. pepo nectaries. Alanine (Ala) accumulated to about 35% of total amino acids in nectaries and nectar during peak secretion; however, alteration of vascular nitrate supply had no impact on Ala accumulation during secretion, suggesting that nectar(y) amino acids are produced by precursors other than nitrate. In addition, nitric oxide (NO) is produced from nitrate and nitrite, at least partially by NR, in nectaries and nectar. Hypoxia-related processes are induced in nectaries during secretion, including lactic acid and ethanolic fermentation. Finally, treatments that alter nitrate supply affect levels of hypoxic metabolites, nectar volume and nectar sugar composition. The induction of N metabolism in C. pepo nectaries thus plays an important role in the synthesis and secretion of nectar sugar.

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The role of alanine synthesis and nitrate-induced nitric oxide production during hypoxia stress in Cucurbita pepo nectaries

Abstract

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Keywords

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