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Title: High spatial resolution mass spectrometry imaging reveals the genetically programmed, developmental modification of the distribution of thylakoid membrane lipids among individual cells of maize leaf

Metabolism in plants is compartmentalized among different tissues, cells and subcellular organelles. Mass spectrometry imaging (MSI) with matrix-assisted laser desorption ionization (MALDI) has recently advanced to allow for the visualization of metabolites at single-cell resolution. Here we applied 5- and 10 μm high spatial resolution MALDI-MSI to the asymmetric Kranz anatomy of Zea mays (maize) leaves to study the differential localization of two major anionic lipids in thylakoid membranes, sulfoquinovosyldiacylglycerols (SQDG) and phosphatidylglycerols (PG). The quantification and localization of SQDG and PG molecular species, among mesophyll (M) and bundle sheath (BS) cells, are compared across the leaf developmental gradient from four maize genotypes (the inbreds B73 and Mo17, and the reciprocal hybrids B73 × Mo17 and Mo17 × B73). SQDG species are uniformly distributed in both photosynthetic cell types, regardless of leaf development or genotype; however, PG shows photosynthetic cell-specific differential localization depending on the genotype and the fatty acyl chain constituent. Overall, 16:1-containing PGs primarily contribute to the thylakoid membranes of M cells, whereas BS chloroplasts are mostly composed of 16:0-containing PGs. Furthermore, PG 32:0 shows genotype-specific differences in cellular distribution, with preferential localization in BS cells for B73, but more uniform distribution between BS and M cells inmore » Mo17. Maternal inheritance is exhibited within the hybrids, such that the localization of PG 32:0 in B73 × Mo17 is similar to the distribution in the B73 parental inbred, whereas that of Mo17 × B73 resembles the Mo17 parent. As a result, this study demonstrates the power of MALDI-MSI to reveal unprecedented insights on metabolic outcomes in multicellular organisms at single-cell resolution.« less
Authors:
 [1] ;  [1] ;  [1] ;  [2] ;  [1] ;  [1]
  1. Ames Lab. and Iowa State Univ., Ames, IA (United States)
  2. Iowa State Univ., Ames, IA (United States)
Publication Date:
Report Number(s):
IS-J-9218
Journal ID: ISSN 0960-7412
Grant/Contract Number:
EEC-0813570; IOS-1354799; AC02-07CH11358
Type:
Accepted Manuscript
Journal Name:
The Plant Journal
Additional Journal Information:
Journal Volume: 89; Journal Issue: 4; Journal ID: ISSN 0960-7412
Publisher:
Society for Experimental Biology
Research Org:
Ames Laboratory (AMES), Ames, IA (United States)
Sponsoring Org:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; mass spectrometry imaging; Kranz anatomy; Zea mays L.; bundle sheath; mesophyll; B73; Mo17; single cell
OSTI Identifier:
1347407
Alternate Identifier(s):
OSTI ID: 1401250

Duenas, Maria Emilia, Klein, Adam T., Alexander, Liza E., Yandeau-Nelson, Marna D., Nikolau, Basil J., and Lee, Young Jin. High spatial resolution mass spectrometry imaging reveals the genetically programmed, developmental modification of the distribution of thylakoid membrane lipids among individual cells of maize leaf. United States: N. p., Web. doi:10.1111/tpj.13422.
Duenas, Maria Emilia, Klein, Adam T., Alexander, Liza E., Yandeau-Nelson, Marna D., Nikolau, Basil J., & Lee, Young Jin. High spatial resolution mass spectrometry imaging reveals the genetically programmed, developmental modification of the distribution of thylakoid membrane lipids among individual cells of maize leaf. United States. doi:10.1111/tpj.13422.
Duenas, Maria Emilia, Klein, Adam T., Alexander, Liza E., Yandeau-Nelson, Marna D., Nikolau, Basil J., and Lee, Young Jin. 2016. "High spatial resolution mass spectrometry imaging reveals the genetically programmed, developmental modification of the distribution of thylakoid membrane lipids among individual cells of maize leaf". United States. doi:10.1111/tpj.13422. https://www.osti.gov/servlets/purl/1347407.
@article{osti_1347407,
title = {High spatial resolution mass spectrometry imaging reveals the genetically programmed, developmental modification of the distribution of thylakoid membrane lipids among individual cells of maize leaf},
author = {Duenas, Maria Emilia and Klein, Adam T. and Alexander, Liza E. and Yandeau-Nelson, Marna D. and Nikolau, Basil J. and Lee, Young Jin},
abstractNote = {Metabolism in plants is compartmentalized among different tissues, cells and subcellular organelles. Mass spectrometry imaging (MSI) with matrix-assisted laser desorption ionization (MALDI) has recently advanced to allow for the visualization of metabolites at single-cell resolution. Here we applied 5- and 10 μm high spatial resolution MALDI-MSI to the asymmetric Kranz anatomy of Zea mays (maize) leaves to study the differential localization of two major anionic lipids in thylakoid membranes, sulfoquinovosyldiacylglycerols (SQDG) and phosphatidylglycerols (PG). The quantification and localization of SQDG and PG molecular species, among mesophyll (M) and bundle sheath (BS) cells, are compared across the leaf developmental gradient from four maize genotypes (the inbreds B73 and Mo17, and the reciprocal hybrids B73 × Mo17 and Mo17 × B73). SQDG species are uniformly distributed in both photosynthetic cell types, regardless of leaf development or genotype; however, PG shows photosynthetic cell-specific differential localization depending on the genotype and the fatty acyl chain constituent. Overall, 16:1-containing PGs primarily contribute to the thylakoid membranes of M cells, whereas BS chloroplasts are mostly composed of 16:0-containing PGs. Furthermore, PG 32:0 shows genotype-specific differences in cellular distribution, with preferential localization in BS cells for B73, but more uniform distribution between BS and M cells in Mo17. Maternal inheritance is exhibited within the hybrids, such that the localization of PG 32:0 in B73 × Mo17 is similar to the distribution in the B73 parental inbred, whereas that of Mo17 × B73 resembles the Mo17 parent. As a result, this study demonstrates the power of MALDI-MSI to reveal unprecedented insights on metabolic outcomes in multicellular organisms at single-cell resolution.},
doi = {10.1111/tpj.13422},
journal = {The Plant Journal},
number = 4,
volume = 89,
place = {United States},
year = {2016},
month = {11}
}

Works referenced in this record:

The developmental dynamics of the maize leaf transcriptome
journal, October 2010
  • Li, Pinghua; Ponnala, Lalit; Gandotra, Neeru
  • Nature Genetics, Vol. 42, Issue 12, p. 1060-1067
  • DOI: 10.1038/ng.703

Genome-wide atlas of transcription during maize development
journal, March 2011