Nicotinate O-Glucosylation Is an Evolutionarily Metabolic Trait Important for Seed Germination under Stress Conditions in Arabidopsis thaliana

L. Wei, F. Zhang, Y. Chang, T. Zhao, M.E. Schranz, M. Wang

Research output: Contribution to journalArticleAcademicpeer-review

15 Citations (Scopus)

Abstract

The glycosylation of nicotinate (NA), a key intermediate of the NAD salvage pathway, occurs widely in land plants. However, the physiological function of NA glycosylation is not well understood in planta, and no gene encoding NA glycosyltransferase has been reported to date. NA glycosylation in Arabidopsis thaliana occurs at either the N- or the O-position of the NA molecule, and O-glucosylation appears to be unique to the Brassicaceae. Using gene-enzyme correlations focused on Family 1 glycosyltransferases (GTs; EC 2.4), we identified and characterized three Arabidopsis GTs, which are likely involved in NA glycosylation. These include one NAOGT (UGT74F2; previously identified as a salicylic acid glycosyltransferases) and two NANGTs (UGT76C4 and UGT76C5). Arabidopsis mutants of UGT74F2 accumulate higher levels of free NA, but not salicylic acid, than that of the wild type, and this inversely correlated with seed germination rates under various abiotic stresses. The germination defect of the ugt74f2-1 mutant could be fully complemented by overexpression of UGT74F2. These observations, together with comprehensive chemical analysis, suggest that NA glycosylation may function to protect plant cells from the toxicity of NA overaccumulation during seed germination. Combined with phylogenetic analysis, our results suggest that NAOGTs arose recently in the Brassicaceae family and may provide a fitness benefit. The multifunctionality of UGT74F2 in Arabidopsis is also investigated and discussed.
Original languageEnglish
Pages (from-to)1907-1924
JournalThe Plant Cell
Volume27
Issue number7
DOIs
Publication statusPublished - 2015

Fingerprint

Niacin
glycosylation
Germination
glycosyltransferases
Arabidopsis
Seeds
seed germination
Arabidopsis thaliana
Glycosylation
Glycosyltransferases
Brassicaceae
salicylic acid
Salicylic Acid
mutants
embryophytes
Plantae
chemical analysis
abiotic stress
Embryophyta
genes

Keywords

  • salicylic-acid glucosyltransferase
  • ugt74f2 glucosyltransferase
  • poly(adp-ribose) polymerase
  • secondary metabolites
  • glandular trichomes
  • nad biosynthesis
  • salvage pathway
  • plants
  • glycosyltransferases
  • trigonelline

Cite this

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title = "Nicotinate O-Glucosylation Is an Evolutionarily Metabolic Trait Important for Seed Germination under Stress Conditions in Arabidopsis thaliana",
abstract = "The glycosylation of nicotinate (NA), a key intermediate of the NAD salvage pathway, occurs widely in land plants. However, the physiological function of NA glycosylation is not well understood in planta, and no gene encoding NA glycosyltransferase has been reported to date. NA glycosylation in Arabidopsis thaliana occurs at either the N- or the O-position of the NA molecule, and O-glucosylation appears to be unique to the Brassicaceae. Using gene-enzyme correlations focused on Family 1 glycosyltransferases (GTs; EC 2.4), we identified and characterized three Arabidopsis GTs, which are likely involved in NA glycosylation. These include one NAOGT (UGT74F2; previously identified as a salicylic acid glycosyltransferases) and two NANGTs (UGT76C4 and UGT76C5). Arabidopsis mutants of UGT74F2 accumulate higher levels of free NA, but not salicylic acid, than that of the wild type, and this inversely correlated with seed germination rates under various abiotic stresses. The germination defect of the ugt74f2-1 mutant could be fully complemented by overexpression of UGT74F2. These observations, together with comprehensive chemical analysis, suggest that NA glycosylation may function to protect plant cells from the toxicity of NA overaccumulation during seed germination. Combined with phylogenetic analysis, our results suggest that NAOGTs arose recently in the Brassicaceae family and may provide a fitness benefit. The multifunctionality of UGT74F2 in Arabidopsis is also investigated and discussed.",
keywords = "salicylic-acid glucosyltransferase, ugt74f2 glucosyltransferase, poly(adp-ribose) polymerase, secondary metabolites, glandular trichomes, nad biosynthesis, salvage pathway, plants, glycosyltransferases, trigonelline",
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year = "2015",
doi = "10.1105/tpc.15.00223",
language = "English",
volume = "27",
pages = "1907--1924",
journal = "The Plant Cell",
issn = "1040-4651",
publisher = "American Society of Plant Biologists",
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}

Nicotinate O-Glucosylation Is an Evolutionarily Metabolic Trait Important for Seed Germination under Stress Conditions in Arabidopsis thaliana. / Wei, L.; Zhang, F.; Chang, Y.; Zhao, T.; Schranz, M.E.; Wang, M.

In: The Plant Cell, Vol. 27, No. 7, 2015, p. 1907-1924.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Nicotinate O-Glucosylation Is an Evolutionarily Metabolic Trait Important for Seed Germination under Stress Conditions in Arabidopsis thaliana

AU - Wei, L.

AU - Zhang, F.

AU - Chang, Y.

AU - Zhao, T.

AU - Schranz, M.E.

AU - Wang, M.

PY - 2015

Y1 - 2015

N2 - The glycosylation of nicotinate (NA), a key intermediate of the NAD salvage pathway, occurs widely in land plants. However, the physiological function of NA glycosylation is not well understood in planta, and no gene encoding NA glycosyltransferase has been reported to date. NA glycosylation in Arabidopsis thaliana occurs at either the N- or the O-position of the NA molecule, and O-glucosylation appears to be unique to the Brassicaceae. Using gene-enzyme correlations focused on Family 1 glycosyltransferases (GTs; EC 2.4), we identified and characterized three Arabidopsis GTs, which are likely involved in NA glycosylation. These include one NAOGT (UGT74F2; previously identified as a salicylic acid glycosyltransferases) and two NANGTs (UGT76C4 and UGT76C5). Arabidopsis mutants of UGT74F2 accumulate higher levels of free NA, but not salicylic acid, than that of the wild type, and this inversely correlated with seed germination rates under various abiotic stresses. The germination defect of the ugt74f2-1 mutant could be fully complemented by overexpression of UGT74F2. These observations, together with comprehensive chemical analysis, suggest that NA glycosylation may function to protect plant cells from the toxicity of NA overaccumulation during seed germination. Combined with phylogenetic analysis, our results suggest that NAOGTs arose recently in the Brassicaceae family and may provide a fitness benefit. The multifunctionality of UGT74F2 in Arabidopsis is also investigated and discussed.

AB - The glycosylation of nicotinate (NA), a key intermediate of the NAD salvage pathway, occurs widely in land plants. However, the physiological function of NA glycosylation is not well understood in planta, and no gene encoding NA glycosyltransferase has been reported to date. NA glycosylation in Arabidopsis thaliana occurs at either the N- or the O-position of the NA molecule, and O-glucosylation appears to be unique to the Brassicaceae. Using gene-enzyme correlations focused on Family 1 glycosyltransferases (GTs; EC 2.4), we identified and characterized three Arabidopsis GTs, which are likely involved in NA glycosylation. These include one NAOGT (UGT74F2; previously identified as a salicylic acid glycosyltransferases) and two NANGTs (UGT76C4 and UGT76C5). Arabidopsis mutants of UGT74F2 accumulate higher levels of free NA, but not salicylic acid, than that of the wild type, and this inversely correlated with seed germination rates under various abiotic stresses. The germination defect of the ugt74f2-1 mutant could be fully complemented by overexpression of UGT74F2. These observations, together with comprehensive chemical analysis, suggest that NA glycosylation may function to protect plant cells from the toxicity of NA overaccumulation during seed germination. Combined with phylogenetic analysis, our results suggest that NAOGTs arose recently in the Brassicaceae family and may provide a fitness benefit. The multifunctionality of UGT74F2 in Arabidopsis is also investigated and discussed.

KW - salicylic-acid glucosyltransferase

KW - ugt74f2 glucosyltransferase

KW - poly(adp-ribose) polymerase

KW - secondary metabolites

KW - glandular trichomes

KW - nad biosynthesis

KW - salvage pathway

KW - plants

KW - glycosyltransferases

KW - trigonelline

U2 - 10.1105/tpc.15.00223

DO - 10.1105/tpc.15.00223

M3 - Article

VL - 27

SP - 1907

EP - 1924

JO - The Plant Cell

JF - The Plant Cell

SN - 1040-4651

IS - 7

ER -