Download Seed Germination and Reserve Mobilization

Seed Germination and
Reserve Mobilization
Secondary article
Article Contents
. Introduction
J Derek Bewley, University of Guelph, Guelph, Ontario, Canada
. Water Uptake
. Onset of Metabolism
When dry seeds take in water, a chain of metabolic events is initiated that results in the
emergence of the radicle, thus completing germination. Thereafter, the major stored
reserves within the seed are mobilized, providing nutrients to support early seedling
growth.
Introduction
Germination incorporates events that commence with the
uptake of water (imbibition) by the quiescent dry seed and
terminates with the emergence of the embryonic axis,
usually the radicle. It is a time of intense metabolic activity,
involving subcellular structural changes, respiration,
macromolecular syntheses and, finally, cell elongation.
Establishment of the seedling occurs following germination, and its growth is initially supported by metabolites
produced by the hydrolysis and conversion of the major
stored reserves, proteins, carbohydrates and oils.
Water Uptake
Uptake of water by a mature dry seed is triphasic (Figure 1).
The initial influx (Phase I, imbibition) is a result of the very
low water potential of the dry matrices of the seed (cell
walls and storage components), which rapidly become
hydrated, resulting in a plateau (Phase II). A further
Germination
Phase I
Postgermination
Phase II
Phase III
Respiration and protein
synthesis commence
Uptake of water
Stored reserves mobilized
Radicle cells elongate
. Completion of Germination
. Reserve Metabolism
increase in water uptake occurs only after germination is
completed, as the embryo grows into a seedling (Phase III).
These kinetics of water uptake are influenced by the
structure of the seed, in that water may not enter all parts
equally, but may be directed preferentially towards the
embryo or its radicle (e.g. in cereals; Hou et al., 1997). The
influx of water into the cells of dry seeds during Phase I
causes temporary structural perturbations, particularly to
membranes, that result in a rapid but temporary leakage of
ions and low-molecular weight metabolites from the seed.
Some seeds may also release proteins (e.g. lectins and
proteinase inhibitors) from the cell walls at this time, and
seed-surface proteins that may serve as protective agents
against bacterial or insect invasion.
The leakage of solutes from cells of the imbibed seed is
symptomatic of a transition of the membrane phospholipid components from the gel phase achieved during
maturation drying to the normal, hydrated crystalline
state (Crowe et al., 1992). The membranes soon resume
their more stable configuration, however, at which time
solute leakage ceases. Presumably, repair to desiccationand rehydration-induced membrane damage is initiated
during imbibition. N-Acylphosphatidylethanolamine
(NAPE), a membrane-stabilizing lipid produced by a
membrane-bound NAPE synthase, increases in imbibing
cotton seeds, and may act to stabilize and enhance cellular
compartmentation (Sandoval et al., 1995).
DNA synthesized
DNA repaired
Cells divide
Proteins synthesized using new mRNAs
Proteins synthesized using extant mRNAs
Mitochondria repaired
Mitochondria synthesized
Solutes leak
Time
Figure 1 The time course of events associated with seed germination and
subsequent postgerminative seedling growth. The time required for the
events to be completed varies from several hours to many weeks,
depending upon inherent genetic factors and the prevailing germination
conditions, particularly temperature and water availability. Based on
Bewley (1997).
Onset of Metabolism
Imbibed seeds rapidly resume metabolic activity. The
essential cellular structures and enzymes for the commencement of metabolism are present within the dry seed,
having survived the desiccation phase that completes seed
maturation.
One of the first activities to resume is respiration, which
can be detected within minutes of the start of imbibition
(Figure 1). The glycolytic and oxidative pentose phosphate
pathways recommence during Phase I, and Krebs’ cycle
enzymes become activated (Botha et al., 1992). Dry seed
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Seed Germination and Reserve Mobilization
tissues contain mitochondria and, although poorly differentiated following maturation drying, they contain sufficient Krebs’ cycle enzymes and terminal oxidases to
produce adequate amounts of ATP to support metabolism
for several hours following imbibition. Subsequently
during germination, two distinct patterns of mitochondrial
development are evident: in starch-storing seeds repair and
activation of preexisting mitochondria occurs, whereas oilstoring seeds typically exhibit mitochondrial biogenesis,
involving both the mitochondrial and nuclear genomes
(Ehrenshaft and Brambl, 1990).
All of the components needed for the resumption of
protein synthesis are present within the cells of mature dry
seeds, although polysomes are absent. Within minutes of
rehydration ribosomes become recruited into polysomal
protein-synthesizing complexes, utilizing mRNAs stored
in the dry seed. Newly synthesized ribosomes are produced
and used within hours of initial polysome assembly and
new transcripts gradually replace those utilized during
early germination; some messages are replaced by identical
ones, but new transcripts are also produced. The majority
of mRNAs are likely to encode proteins essential for the
support of normal cellular metabolism, i.e. ‘growth
maintenance’ processes that are not unique to germination
(Bewley and Marcus, 1990). New proteins are synthesized
as germination proceeds including cell regulators such as
protein kinases, H 1 ATPases and 14-3-3 proteins (Bradford et al., 2000; Testerink et al., 1999).
Completion of Germination
Radicle protrusion through the structures surrounding the
embryo is the usual event that terminates germination and
marks the beginning of seedling growth. This occurs as a
result of cell extension, which may or may not be
accompanied by cell division. Synthesis of DNA occurs
in the radicle cells soon after the start of imbibition
(Figure 1), to repair damage to the macromolecule sustained
during desiccation and rehydration, as well as synthesis of
mitochondrial DNA. A second period of DNA synthesis
occurs after radicle protrusion, along with an increase in btubulin, a microtubule component associated with cell
division, although in some seeds these events may slightly
precede cell elongation (de Castro et al., 1995).
Emergence of the radicle by cell extension is a turgordriven process. The radicle cell walls must become more
stretchable, and thus wall loosening could result from the
activity of certain proteins, expansins, which disrupt the
hydrogen bonds linking cell wall polymers (e.g. matrix
polysaccharides and cellulose microfibrils) (Cosgrove,
1997). These proteins are present in germinating seeds,
but their relationship to radicle extension remains to be
determined.
2
In some seeds, the embryo is surrounded by an
endosperm or perisperm or, in conifers, a megagametophyte, which is sufficiently rigid to prevent extension of the
radicle and completion of germination. In embryos that do
not suffer such constraints the turgor potential (Cr) of the
radicle cells is sufficient to stretch their walls and drive their
elongation. In those that are constrained by a surrounding
structure, which frequently has thickened hemicellulosecontaining cell walls, a decline in their resistance must
occur concurrently with radicle elongation. This might be
achieved by cell wall hydrolases, such as cellulase,
glucanase, the hemicellulases endo-b-mannanase and
arabinosidase, or cell-separating enzymes like the polygalacturonases. A causal link between germination and
enzymic weakening the cell walls of the surrounding
structures remains to be established in most seeds, however
(Bewley, 1997; Bradford et al., 2000).
Reserve Metabolism
The major mobilization of stored reserves in the storage
organs commences after the completion of germination,
and supports growth of the seedling until it becomes
photosynthetically active (autotrophic). Some mobilization can occur in the radicle and plumule before germination is completed, and might be important for early axis
growth.
As the high-molecular-weight reserves contained within
the seed storage organs (usually the cotyledons or
endosperm) are mobilized they are converted into easily
transportable low-molecular-weight metabolites that are
readily moved to the growing regions in support of the
energy-producing and synthetic events therein (Figure 2).
Seed storage organs contain substantial quantities of two
or more of the major reserves, carbohydrates, oils and
proteins, and the hydrolysis and utilization of these usually
occurs concurrently.
Carbohydrates
Starch is the most common reserve carbohydrate in seeds
and an important commercial source is the endosperm of
cereals, e.g. wheat, barley and maize. The amylose and
amylopectin in the native starch grain are first hydrolysed
by a-amylase, which randomly breaks the a (1!4)
glycosidic links between the glucose (Glc) residues. Starch
degradation is aided by b-amylase, which cleaves off
successive disaccharide maltose units (Glc-Glc) from the
nonreducing end of the large oligomers released by prior aamylolytic attacks. These enzymes produce Glc and
maltose from amylose and, in addition, highly branched
short chains of Glc, called limit dextrins, from amylopectin. A debranching enzyme (limit dextrinase) releases the
short chains by hydrolysing the a (1!6) branch points,
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Seed Germination and Reserve Mobilization
First leaf
STARCH
Aleurone layer
Starchy
endosperm
Scutellum
Amylopectin
Branched α(1→ 4) and α(1→6)Glc
Protein
α-A mylase
Starch
GA
Sucrose
Gln
Asn
Hydrolases
Peptides +
Glucose
amino acids
Amylose
Linear α(1→ 4)Glc
Large branched oligomers
of Glc
Large linear oligomers
of Glc
α- and β-A mylase
Glc, maltose and
limit dextrins
Roots
Glc and maltose
α- and β-A mylase,
limit dextrinase
Endosperm
Figure 2 Diagrammatic representation of the major events taking place
during mobilization in a young cereal (barley) seedling following
germination.
The plant hormone gibberellic acid (GA) is released from the scutellum
and diffuses to the living cells of the aleurone layer where it promotes the
synthesis of several hydrolytic enzymes. These are secreted into the
nonliving cells of the starchy endosperm where the starch and protein
reserves are stored. a-Amylase and maltase are key enzymes in the
degradation of starch (see Figure 3) to glucose, and the proteinases
hydrolyse proteins to short peptides and amino acids. The hydrolytic
products are absorbed by the scutellum, which is part of the growing embryo.
There the glucose is converted to sucrose, and the products of protein
mobilization to the amino acids glutamine (Gln) and asparagine (Asn). These
are transported throughout the seedling via the vascular system as a supply of
nutrients to support growth.
which are further cleaved by the amylases. Maltose is
converted to its constituent Glc units by maltase (Figure 3).
This mode of starch breakdown is common in cereals,
where the a-amylase, debranching enzyme and maltase are
synthesized in, and released from, the embryo (scutellum)
and surrounding aleurone layer into the nonliving storage
cells of the starchy endosperm following germination; bamylase is already present in the latter at grain maturity,
and is activated when required. The resultant Glc is taken
up into the growing embryo via the scutellum and is
converted to sucrose for transport to, and utilization by,
the growing regions of the developing seedling.
Maltase
Glc
Embryo
Sucrose
Sucrose synthesizing
enzymes
Transport to growing regions of seedling
Figure 3 Hydrolysis of starch grains in cereals by amylolysis. In legumes
amylose and amylopectin may be converted initially to glucose 1phosphate (Glc-1-P), maltose and limit dextrins by starch phosphorylase
and b-amylase, and then further to glucose (Glc) by limit dextrinase, bamylase and maltase.
In some dicot seeds, breakdown of starch involves
phosphorolysis, rather than amylolysis, and starch phosphorylase, which introduces a phosphate moiety across the
a (1!4) linkage between the penultimate and last Glc at
the nonreducing end of the polysaccharide chain, replaces
a-amylase as the main degradative enzyme. The other
enzymes are still required to achieve full hydrolysis of the
starch. In pea cotyledons, the enzymes are produced within
the living storage cells themselves, and sucrose is also
synthesized therein for transport to the growing axes.
Seeds of some species, including the endospermic
legumes (e.g. carob, fenugreek, guar), ivory nut, date and
coffee store hemicelluloses in the cell walls of the
extraembryonic storage tissues (endosperm or perisperm),
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Seed Germination and Reserve Mobilization
which are frequently nonliving at maturity. The most
prevalent storage hemicelluloses have a b (1!4)-linked
mannose (Man) backbone (mannans), with a (1!6)-linked
unit side-chains of galactose (Gal) and/or glucose.
Enzymes released from an aleurone layer, when present,
or from the embryo are responsible for the mobilization of
the stored reserves following germination. Endo-b-mannanase is the endoenzyme that hydrolyses polymers of
Man (tetramers or larger) to mannobiose or mannotriose,
and b-mannoside mannohydrolase then converts these
residues to Man. a-Galactosidase and a-glucosidase
release the Gal and Glc side-chains. The Man, Glc and
Gal are transported to the embryo, where they are
phosphorylated and converted to sucrose to support
seedling growth. Excessive sucrose production leads to
the temporary synthesis of starch in the cotyledons, which
is remobilized when sugar content declines.
Protein
The hydrolysis of storage proteins (polypeptides) to their
constituent amino acids is effected by proteinases, which
are categorized in relation to their hydrolytic activity.
Endopeptidases cleave internal peptide bonds to yield
smaller oligopeptides, which are hydrolysed further by
peptidases to yield amino acids. Aminopeptidases and
carboxypeptidases cleave the terminal amino acid from the
free amino or carboxyl end, respectively, of a protein or
oligopeptide chain (Scheme 1).
In cereal grains, the major site of storage proteins is the
nonliving endosperm, and proteinases and peptidases
synthesized and secreted by the aleurone layer following
germination contribute substantially to their mobilization.
There are also preformed proteinases within the endosperm of mature dry grains that become activated
following hydration. The low-molecular weight products
of endosperm protein hydrolysis are actively taken up by
the scutellum, small peptides are hydrolysed, and the
resultant amino acids are transported, along with those
taken up from the endosperm, to the growing axes, usually
following conversion to the amides, glutamine and
asparagine.
In most dicot seeds the storage proteins are present in
distinct protein bodies within the cotyledons. Initially
following germination a ‘proteinase A’ class of hydrolases,
Storage protein
Carboxypeptidases
Amino acids
Aminopeptidases
Endopeptidases
Peptidases
Oligopeptides
Scheme 1 Hydrolysis of storage proteins to their constituent amino acids
by proteinases.
4
usually endopeptidases, cleave short-chain peptides from
the storage proteins, rendering them soluble, and susceptible to further proteolysis. Endopeptidases of a ‘proteinase B’ class and carboxypeptidases are then able to
hydrolyse the modified storage proteins to produce small
oligopeptides and amino acids. These reactions occur
within the protein bodies; oligopeptides released therefrom
into the cytoplasm are further degraded to amino acids by
aminopeptidases and peptidases capable of hydrolysing diand tripeptides (Figure 4). Conversion of the amino acids to
glutamine and asparagine occurs prior to their translocation to the seedling axes.
The proteolytic enzymes active within the protein bodies
are synthesized on the endoplasmic reticulum (ER),
inserted into the ER lumen and packaged into vesicles.
These are transported to the protein bodies, with which
they fuse, releasing the hydrolases into contact with the
storage proteins. As protein digestion proceeds, the
emptying protein bodies fuse to form large vacuoles into
which a variety of hydrolases are secreted, and they become
autophagic vesicles responsible for the senescence and
ultimate degeneration of the expended cotyledons (Herman et al., 1981).
Oils
Triacylglycerols (TAGs) are the major storage oils in seeds.
Catabolism of the TAGs involves three discrete organelles
present within the oil-storing cells:
1. the TAG-storing oil body where hydrolysis of TAGs
to free fatty acids (FFA) and glycerol commences;
Protein body
Cytosol
Amino acids
A
Amides
Axes
A+B
Am + Ps
+C
Storage
protein
Oligopeptides
Cotyledons
Figure 4 A generalized pathway for the mobilization of storage proteins
in the protein bodies of dicot seeds. The native storage protein, here a
disulfide-linked insoluble legumin, is initially trimmed by proteinase A
(endopeptidase) activity (A) to render it more soluble as small
oligopeptides are released. Further proteinase A activity, and that of
proteinase B endopeptidases (A and B) result in hydrolysis of the protein to
amino acids and small peptides which are transported into the cytosol.
Hydrolysis of the polypeptides in the protein bodies is aided by the
carboxypeptidases (C). The released oligopeptides are degraded further by
aminopeptidases (Am) and peptidases (di- and tripeptidases, Ps) within the
cytosol to yield amino acids. These are converted to the amides, glutamine
and asparagine, and transported to the growing axes to support seedling
growth. Based on Wilson (1986).
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Seed Germination and Reserve Mobilization
Oil body
(i)
(1)
TAG
(1)
Gly +
FFA
Gly +
+ MAG
FFA
ATP
ADP
Gly
+
(1)
Glyoxysome
FFA
CoA
(2)
Acyl CoA
FFA
NADH
NAD
Cytoplasm
α Gly P
Gly
AMP
ATP
(3)
FADH
(11)
Oxaloacetate
Malate
CoA
(10)
Isocitrate
(8)
Acetyl CoA
NAD
NADH
(6)
β-Ketoacyl–CoA
Mitochondrion
(13)
NADH
NAD
(14)
Fumarate
FADH
(5)
CoA
Succinate
FAD
H2O
+
1/2 O2
β-OH-acyl–CoA
Acyl (cn-2)–CoA
Citrate
(9)
(12)
(4)
(7)
Acetyl–CoA
Glyoxylate
O2
Crotonyl–CoA
β-Oxidation
Glyoxylate
Cycle
H2O2
FAD
Malate
α-Gly P
(ii)
Oxaloacetate
(15)
DHAP
NAD
(15)
(26)
UDPGIc
Fructose (or Fru-6-P)
Sucrose (to embryo
or vacuole)
Oxaloacetate
GTP
PPi
(25)
Cytoplasm
NADH
(16)
GDP
UTP
CO2
Glc-1-P
PEP
(24)
(17)
Glc-6-P
2PGA
(18)
(23)
3PGA
G-3-P
NAD
(21)
Fru-6-P
(22)
FruDP
G3P
(19)
NADH
(20)
ATP
DPGA
ADP
DHAP
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Seed Germination and Reserve Mobilization
Triacylglycerol
Diacylglycerol + FFA
Monoacylglycerol + 2FFA
Glycerol + 3FFA
Scheme 2 Initial triacylglycerol hydrolysis by lipases.
2. the glyoxysome, where the FFA are oxidized, and
synthesis of succinate occurs via the glyoxylate cycle;
3. the mitochondrion, in which succinate is converted to
malate or oxaloacetate. The latter two are processed
further in the cytosol to yield sucrose (Figure 5).
Initial TAG hydrolysis (lipolysis) is by lipases, which
hydrolytically cleave the fatty acids from the glycerol
backbone according to Scheme 2.
Glycerol eventually enters the glycolytic pathway in the
cytosol following its phosphorylation, and by the reversal
of glycolysis is converted to hexoses.
The free fatty acids (FFA) pass from the oil body to the
glyoxysome, an organelle which is present in a nascent
form in most mature dry oil-storing seeds, and enlarges as
its membranes become augmented with phospholipids and
its matrix with enzymes.
In the glyoxysome, the FFA are subjected to the
sequential removal of acetyl–CoA moieties by b-oxidation, with the involvement of additional enzymes if the
FFA are unsaturated or contain an odd number of C atoms
(Bewley and Black, 1994). Directly coupled to the boxidation pathway is the glyoxylate cycle, which takes the
acetyl–CoA and in a series of enzymatic reactions links this
via enzymes in the mitochondria to the cytosolic glycolytic
pathway, which then operates to produce hexose (Figure 5).
The key enzymes in the glyoxysome are isocitrate lyase (IL)
and malate synthase (MS), which produce succinate and
malate, respectively, for further processing in the mitochondria and cytosol.
The final steps in the conversion of FFA and glycerol
occur in the cytosol, where the hexoses are converted to
sucrose, which is transported to and within the growing
seedling. In some storage tissues the acetyl–CoA arising
from b-oxidation of FFA can be utilized for amino acid
synthesis via partial reactions of the glyoxylate and Krebs’
cycle. In nonpersistent storage tissues the glyoxysomes
degenerate as the cells become depleted and senesce, but in
cotyledons that turn green and persist during seedling
growth their enzyme complement changes as they become
converted to peroxisomes; these play an important role in
photorespiration.
References
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Germination, 2nd edn. New York: Plenum Press.
Bewley JD and Marcus M (1990) Gene expression in seed development
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Botha FC, Potgeiter GP and Botha A-M (1992) Respiratory metabolism
and gene expression during seed germination. Journal of Plant Growth
Regulation 11: 211–224.
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radicle emergence in imbibed tomato seeds. In: Black M, Bradford KJ
and Vasquez-Ramos J (eds) Advances and Applications in Seed
Biology. Proceedings of the 6th International Workshop on Seeds, pp.
231–251.
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molecular bases of extensible cell walls and cell enlargement. Plant Cell
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Review of Physiology 54: 579–599.
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(1995) b-Tubulin accumulation and DNA replication in imbibing
tomato seeds. Plant Physiology 109: 499–504.
Ehrenshaft M and Brambl R (1990) Respiration and mitochondrial
biogenesis in germinating embryos of maize. Plant Physiology 93: 295–304.
Herman EM, Baumgartner B and Chrispeels MJ (1981) Uptake and
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Hou JQ, Kendall EJ and Simpson GM (1997) Water uptake and
distribution in non-dormant and dormant wild oat (Avena fatua L.)
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(1995) N-Acylphosphatidylethanolamine in dry and imbibing cotton
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Physiology 109: 269–275.
Testerink C, van der Meulen RM, Oppeijk BJ et al. (1999) Differences in
spatial expression between 14-3-3 isoforms in germinating barley
embryos. Plant Physiology 121: 81–87.
Figure 5 Pathways of triacylglycerol (TAG) catabolism and hexose assimilation. Enzymes: 1, lipases; 2, fatty acid thiokinase; 3, acyl–CoA dehydrogenase;
4, enoyl–CoA hydratase (crotonase); 5, b-hydroxyacyl–CoA dehydrogenase; 6, b-ketoacyl thiolase; 7, citrate synthetase; 8, aconitase; 9, isocitrate lyase;
10, malate synthetase; 11, malate dehydrogenase; 12, catalase; 13, succinate dehydrogenase; 14, fumarase; 15, malate dehydrogenase; 16,
phosphoenolpyruvate carboxykinase; 17, enolase; 18, phosphoglycerate mutase; 19, phosphoglycerate kinase; 20, glyceraldehyde-3-phosphate
dehydrogenase; 21, aldolase; 22, fructose-1,6-bisphosphatase; 23, phosphohexoisomerase; 24, phosphoglucomutase; 25, UDPGlc pyrophosphorylase;
26, sucrose synthetase or sucrose-6-P synthetase and sucrose phosphate. (i) Glycerol kinase; (ii) a-glycerol phosphate oxidoreductase. Substrates TAG,
triacylglycerol; MAG, monoacylglycerol; Gly, glycerol; FFA, free fatty acid; PEP, phosphoenolpyruvate; 2PGA, 2-phosphoglyceric acid; 3PGA, 3phosphoglyceric acid; DPGA, 1,3-diphosphoglyceric acid; G3P, glyceraldehyde 3-phosphate; FruDP, fructose 1,6-bisphosphate; Fru-6-P, fructose 6phosphate; Glc-6-P, glucose 6-phosphate; Glc-1-P, glucose 1-phosphate; UDPGlc, uridine diphosphoglucose; a-Gly P, a-glycerol phosphate; DHAP,
dihydroxyacetone phosphatase. Coenzymes and energy suppliers: FAD(H), flavin adenine dinucleotide (reduced); NAD(H), nicotinamide adenine
dinucleotide (reduced); GTP, guanosine triphosphate; ATP, adenosine triphosphate; UTP, uridine triphosphate; GDP, guanosine diphosphate; ADP,
adenosine diphosphate; AMP, adenosine monophosphate; CoA, coenzyme A. Based on Bewley and Black (1994).
6
ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Nature Publishing Group / www.els.net
Seed Germination and Reserve Mobilization
Wilson KA (1986) Role of proteolytic enzymes in the mobilization of
protein reserves. In: Dalling MJ (ed.) Plant Proteolytic Enzymes, vol.
2, pp. 19–47. Boca Raton, FL: CRC Press.
Further Reading
Dennis DT, Turpin DH, Lefebvre DD and Layzell DB (eds) (1997) Plant
Metabolism, 2nd edn. Harlow, UK: Addison-Wesley Longman.
Shewry PR and Casey R (eds) (1999) Seed Proteins. Dordrecht: Kluwer
Academic.
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