P 450 variations bifurcate the early terpene indole alkaloid pathway in Catharanthus roseus and Camptotheca acuminata
Author
Miller, Justin C.
Department of Chemistry, University of Illinois at Urbana-Champaign, 1201 W. Gregory Dr., 162 Edward R. Madigan Laboratory (ERML), Urbana, IL, 61801, USA
Author
Hollatz, Allison J.
Author
Schuler, Mary A.
text
Phytochemistry
2021
112626
2021-03-31
183
1
13
http://dx.doi.org/10.1016/j.phytochem.2020.112626
journal article
10.1016/j.phytochem.2020.112626
1873-3700
8291734
2.5. In vitro reconstitution of
Camptotheca SLAS
activities
For subsequent
in vitro
reconstitution assays, the His
6
-tagged
Camptotheca
CYP
72A564, CYP72A565 and CYP72A730 and
Catharanthus
CYP
72A1v3 ORFs were cloned into the IPTG-inducible pCW bacterial expression vector and their full-length proteins were purified from
E. coli
as outlined in the experimental procedures. His
6
-tagged full-length membrane-bound forms of
Camptotheca
CPR
1 (His
6
CPR1full) and CPR2 (His
6
CPR2full) as well as truncated soluble forms of these electron transfer proteins (His
6
CPR1Δ48, His
6
CPR2Δ68) were cloned into the IPTG-inducible pET28 bacterial expression vector and purified from
E. coli
. Reduced carbon monoxide difference spectra (
Omura and Sato, 1967
) used to quantify P450 levels indicated that all three
Camptotheca
His
6
-tagged CYP72A proteins were mixtures of properly folded protein (peak around
450 nm
) with some free heme from misfolded protein (peak around
420 nm
) (
Fig. S7
). The calculated P450 concentrations for these
Camptotheca
preparations were in the micromolar range (15.9 μM for CYP72A564, 31.9 μM for CYP72A565, 3.34 μM for CYP72A730). Cytochrome
c
reduction assays (
Guengerich et al., 2009
) used to quantify CPR activities indicated that the full-length and truncated His
6
--tagged CPR1 proteins efficiently reduced cytochrome
c
whereas the full-length and truncated His
6
-tagged CPR2 proteins inefficiently reduced cytochrome
c
at equivalent protein levels (
Fig. S8
).
Reconstitution of the purified His
6
-tagged CYP72A564 and CYP72A565 proteins with His
6
CPR1full and DLPC showed that both of these
Camptotheca
P450s metabolize loganic acid and loganin in the presence of NADPH (
Fig. 4A and B
,
5
). For both proteins, products from loganic acid include significant amounts of secologanic acid and smaller amounts of secoxyloganic acid—an overoxidation of the aldehyde to a carboxylic acid. Both proteins also produced secologanin from loganin. Similar reconstitutions of these two
Camptotheca
P450s with His
6
CPR2full showed no detectable conversion of loganic acid or loganin (
Fig. 4C and D
); reconstitutions with His
6
CPR1Δ48 and His
6
CPR2Δ68 showed no conversion of loganin or loganic acid (data not shown). Reconstitutions of the more divergent CYP72A730 with His
6
CPR1full showed no conversion of loganic acid or loganin (
Fig. 4A and B
,
5
). Reconstitutions with full-length
Catharanthu
s CYP72A1v3 showed conversion of loganin to secologanin but not conversion of loganic acid (
Fig. 4A and B
,
5
).
Lacking access to the 7-deoxyloganic acid needed to assess the 7-hydroxylation activity of these CYPs reported by
Yang et al. (2019)
, we assayed the structurally-related geniposide listed as an alternate substrate. Although we observed product formation consistent with geniposide hydroxylation for CYP72A1, CYP72A564, and CYP72A565 reconstituted with
Camptotheca
His
6
CPR1full, no such activity was observed for CYP72A730 (Supplemental Fig. S13).