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Plant Physiol, February 2002, Vol. 128, pp. 428-438
Differential Substrate Inhibition Couples Kinetically Distinct
4-Coumarate:Coenzyme A Ligases with Spatially Distinct Metabolic Roles
in Quaking Aspen1
Scott A.
Harding,
Jacqueline
Leshkevich,
Vincent L.
Chiang, and
Chung-Jui
Tsai*
Plant Biotechnology Research Center, School of Forestry and Wood
Products, Michigan Technological University, Houghton, Michigan 49931
4-Coumarate:coenzyme A ligase (4CL) activates
hydroxycinnamates for entry into phenylpropanoid branchways that
support various metabolic activities, including lignification and
flavonoid biosynthesis. However, it is not clear whether and how
4CL proteins with their broad substrate specificities fulfill the
specific hydroxycinnamate requirements of the branchways they supply.
Two tissue-specific 4CLs, Pt4CL1 and Pt4CL2, have previously been
cloned from quaking aspen (Populus tremuloides Michx.),
but whether they are catalytically adapted for the distinctive
metabolic roles they are thought to support is not apparent from
published biochemical data. Therefore, single- and mixed-substrate
assays were conducted to determine whether the 4CLs from aspen exhibit
clear catalytic identities under certain metabolic circumstances.
Recombinant Pt4CL1 and Pt4CL2 exhibited the expected preference for
p-coumarate in single-substrate assays, but strong
competitive inhibition favored utilization of caffeate and
p-coumarate, respectively, in mixed-substrate assays.
The Pt4CL1 product, caffeoyl-CoA, predominated in mixed-substrate assays with xylem extract, and this was consistent with the near absence of Pt4CL2 expression in xylem tissue as
determined by in situ hybridization. It is interesting that the Pt4CL2
product p-coumaroyl-CoA predominated in assays with
developing leaf extract, although in situ hybridization revealed that
both genes were coexpressed. The xylem extract and recombinant 4CL1
data allow us to advance a mechanism by which 4CL1 can selectively
utilize caffeate for the support of monolignol biosynthesis in maturing
xylem and phloem fibers. Loblolly pine (Pinus taeda), in
contrast, possesses a single 4CL protein exhibiting broad substrate
specificity in mixed-substrate assays. We discuss these 4CL differences
in terms of the contrasts in lignification between angiosperm trees and
their gymnosperm progenitors.
1
This work was supported in part by State of
Michigan Research Excellence Funds and by the U.S. Department of
Agriculture McIntire-Stennis Forestry Research Program.
*
Corresponding author; e-mail chtsai{at}mtu.edu; fax 906-487-2915.
© 2002 American Society of Plant Physiologists
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