Plant Molecular Biology 40: 267–278, 1999.
© 1999 Kluwer Academic Publishers. Printed in the Netherlands.
Diverse range of gene activity during Arabidopsis thaliana leaf senescence
includes pathogen-independent induction of defense-related genes
Betania F. Quirino
, Jennifer Normanly
and Richard M. Amasino
Department of Biochemistry, University of Wisconsin, 433 Babckock Drive, Madison, W1 53706, USA (
Department of Biochemistry and Molecular Biology, University of Massachusetts, Amherst,
MA 01003, USA
Received 19 October 1998; accepted in revised form 20 January 1999
Key words: defense, gene expression, leaf senescence, nitrilase, pathogen-free, salicylic acid
To determine the range of gene activities associated with leaf senescence, we have identiﬁed genes that show
preferential transcript accumulation during this developmental stage. The mRNA levels of a diverse array of
gene products increases during leaf senescence, including a protease, a ribosomal protein, two cinnamyl alcohol
dehydrogenases, a nitrilase and glyoxalase II. Two of the genes identiﬁed are known to be pathogen-induced.
The senescence speciﬁcity of each gene was determined by characterization of transcript accumulation during leaf
development and in different tissues. The increased expression of nitrilase in senescent leaves is paralleled by
an increase in free indole-3-acetic acid (IAA) levels. Additionally, we have demonstrated that the induction of
defense-related genes during leaf senescence is pathogen-independent and that salicylic acid accumulation is not
essential for this induction. Our data indicate that the induction of certain genes involved in plant defense responses
is a component of the leaf senescence program.
Senescence is the ﬁnal episode of leaf development.
During this stage, nutrients contained in the leaf are
distributed to other parts of the plant before the leaf
dies (Leopold, 1961). Leaf senescence is thought to
be of great adaptive value because nutrients, which
are often present in limiting amounts in the soil, are
retained by the plant instead of being lost to the
environment (Vitousek and Howarth, 1991).
Leaf senescence is an organized developmental
program. At the cellular level, organelles are dis-
assembled in a precise hierarchy. Chloroplasts are
the ﬁrst to be affected during the senescence pro-
gram while the nucleus and mitochondria are last
(Smart, 1994; Thomson and Platt-Aloia, 1987). The
chlorophyll, lipid, protein and RNA content of the
leaf declines as senescence progresses (Matile, 1992;
The nucleotide sequence data reported will appear in the Gen-
Bank database under the accession numbers AF118822 (SAG24),
AF118823 (SAG26) and AF118824 (SAG29).
Koiwa et al., 1981; Lohman et al., 1994). Although
the molecular mechanisms of leaf senescence are not
well understood, it is clear that during leaf senescence
a number of catabolic pathways increase in activity
(for a review, see Weaver et al., 1997).
Analysis of gene expression and determination of
the function of gene products that increase during
leaf senescence is one strategy that can be used to
increase our understanding of this complex develop-
mental stage. To date gene expression during leaf
senescence has been analyzed in a number of species
such as Arabidopsis thaliana (Lohman et al., 1994;
Hensel et al., 1993; Taylor et al., 1993; Park et al.,
1998; Bernhard and Matila, 1994), Brassica napus
(Buchanan-Wollaston and Ainsworth, 1997; Hanfrey
et al., 1996; Buchanan-Wollaston et al., 1994), maize
(Smart et al., 1995), barley (Kleber-Janke and Krupin-
ska, 1997; Becker and Apel, 1993) and tomato (John
et al., 1997; Davies and Grierson, 1989) (for a review
see Buchanan-Wollaston, 1997). However, despite
the intense activity in the ﬁeld, the studies have not