Changes to the proteome and targeted metabolites of
xylem sap in Brassica oleracea in response to salt stress
N. FERNANDEZ-GARCIA,
1
M. HERNANDEZ,
1
J. CASADO-VELA
2
*, R. BRU,
3
F. ELORTZA,
2
P. HEDDEN
4
&
E. OLMOS
1
1
Department of Abiotic Stress and Plant Pathology. CEBAS-CSIC. P.O. Box 164. Murcia,
2
Proteomics Platform, CIC
bioGUNE, CIBERehd, ProteoRed. Bizkaia Technology Park, Building 800, 48160, Bizkaia,
3
Proteomics and Functional
Genomics Group. ProteoRed. Departamento de Agroquímica y Bioquímica, Facultad de Ciencias, Universidad de Alicante,
Spain and
4
Department of Plant Science. Rothamsted Research, Harpenden AL5 2JQ, Herts, UK
ABSTRACT
Root-to-shoot signalling via xylem sap is an important
mechanism by which plants respond to stress. This signal-
ling could be mediated by alteration in the concentrations
of inorganic and/or organic molecules.
The effect of salt stress on the contents of xylem sap in
Brassica olarecea has been analysed by mass spectrometry
in order to quantify these changes. Subcellular location
of arabinogalactan proteins (AGPs) by immunogold
labelling and peroxidase isozymes was also analysed by
isoelectrofocusing.
The xylem sap metabolome analysis demonstrated the
presence of many organic compounds such as sugars,
organic acids and amino acids. Of these, amino acid con-
centrations, particularly that of glutamine, the major amino
acid in the sap, were substantially reduced by salt stress. The
xylem sap proteome analysis demonstrated the accumula-
tion of enzymes involved in xylem differentiation and ligni-
fication, such as cystein proteinases, acid peroxidases, and
a putative hydroxycinnamoyl-CoA:shikimate hydroxycin-
namoyl transferase under salt stress. The peroxidase
isozyme pattern showed that salt stress induced a high
accumulation of an acid isoform.
These results suggest that xylem differentiation and
lignification is induced by salt stress. The combination of
different methods to analyse the xylem sap composition
provides new insights into mechanisms in plant develop-
ment and signalling under salt stress.
Key-words: arabinogalactan proteins; cystein proteinases;
lignification; peroxidases; programmed cell death; phi cells;
xylem differentiation.
INTRODUCTION
The movement of solutes from roots to the aerial parts
of the plant is accomplished by the tracheary elements of
the xylem, which was traditionally considered as the
main conduit for water and minerals. Structurally the xylem
is a complex tissue containing at least tracheary elements
and parenchyma cells and other cell-types that function as
supporting cells (Evert 2007). On the other hand, sieve
tubes of phloem are the main pathway to transport the
photosynthetic assimilates from leaves to fruits, roots
and buds.
Probably for these reasons, xylem sap analysis has focused
mainly on the mineral contents. However, xylem sap con-
tains also organic solutes, including carbohydrates, amino
acids, organic acids, hormones and proteins (Satoh 2006).
Transport via the xylem could supply signal molecules other
than water and nutrient from the root system and that
modification in the concentrations of these signals under
abiotic stress can play important roles in plant adaptation
to stress (Dodd 2005). Differences in the concentrations
of organic compounds in xylem sap from stressed and
unstressed plants have been found for a number of species
(Gollan, Schurr & Schulze 1992; Patonnier, Peltier & Marigo
1999; Chen et al. 2001; De Sousa & Sodek 2003; Albacete
et al. 2009). Xylem sap analysis under salt stress focused
mainly on the role of hormone signalling mediated by absci-
sic acid (ABA) (Wolf,Jeschke & Hartung 1990;Zhao,Munns
& King 1991; Gomez-Cadenas et al. 1998; Chen et al. 2001;
Albacete et al. 2009). However, detailed studies of other
organic compounds such as sugars,organic acids,amino acids
or proteins in xylem sap and the quantification of changes
under salt stress are scarce in the literature.
In the last 5 years, there have been considerable advances
in xylem sap analysis using proteomic approaches. The
xylem sap proteomes of Zea mays, Brassica napus, Glycine
max, Vitis vinifera and Populus have been studied using
separation in 2D gel electrophoresis and mass spectromet-
ric identification (Kehr, Buhtz & Giavalisco 2005; Alvarez
et al. 2006; Djordjevic et al. 2007; Agüero et al. 2008;
Aki et al. 2008; Dafoe & Constabel 2009). Xylem sap pro-
teome analysis shows similar groups of proteins present
in the different species investigated (Buhtz et al. 2004;
Dafoe & Constabel 2009). These groups of proteins were
classified as proteins involved in cell wall metabolism and
remodelling (glycosyl hydrolases, arabino-furanosidases,
Correspondence: E. Olmos. Fax: +34 968 396213; e-mail: eolmos@
cebas.csic.es
*Current address: Translational Oncology Unit, Centro Nacional
de Biotecnología, lab. 35. C/ Darwin 3, Madrid, Spain.
Plant, Cell and Environment (2011) 34, 821–836 doi: 10.1111/j.1365-3040.2011.02285.x
© 2011 Blackwell Publishing Ltd 821