Supporting Information Tables S1 & S2, Notes S1–S4
Volatile isoprenoid emissions from plastid to planet
Sandy P. Harrison, Catherine Morfopoulos, K. G. Srikanta Dani, I. Colin Prentice, Almut Arneth,
Brian J. Atwell, Michael P. Barkley, Michelle R. Leishman, Francesco Loreto, Belinda E. Medlyn,
Ülo Niinemets, Malcolm Possell, Josep Peñuelas and Ian J. Wright
The Supporting Information contains descriptions of the data sources and analytical methods,
including Notes S1, information about the sources of values of the Michaelis-Menten constants
(Km) used in constructing Fig. 1 (Table S1); Notes S2, information on the trait and isoprene
database; Notes S3, a summary of the observational or experimental evidence for lags in isoprenoid
emissions from the published literature (Table S2); and Notes S4 information about the remotelysensed data used in the analysis of the controls on isoprene emission at a regional scale; and Notes
S5, References.
Notes S1 Source of Km data
The Km data used in Fig. 1 were derived from published literature as detailed in the Table S1 below.
Table S1 Information on Km values
Km
superscript
in Figure 1
Enzyme
Source organism
Reference
A
1-deoxy-D-xylulose 5phosphate synthase
Rhodobacter capsulatus
Eubanks and Dale-Poulter, 2003
B
1-deoxy-D-xylulose-5phosphate reductoisomerase
(aka: CM synthase)
Arabidopsis thaliana
Rohdich et al., 2006
Escherichia coli
Richard et al., 2004
Aquifex aeolicus
Sgraja et al., 2008
C
D
2-C-methyl-D-erythritol 4phosphate cytidylyl
transferase
4-diphosphocytidyl-2-Cmethylerythritol kinase
E
2C-methyl-D-erythritol 2,4cyclodiphosphate synthase
Mycobacterium
tuberculosis
Geist et al., 2010
F
1-hydroxy-2-methyl-2-(E)butenyl 4-diphosphate
synthase
Escherichia coli
Zepeck et al., 2005
G
1-hydroxy-2-methyl-2-(E)butenyl 4-diphosphate
reductase
Aquifex aeolicus
Altincicek et al., 2002
H
Isopentenyl diphosphate
isomerase
Cinchona robusta
Ramos-Valdivia et al., 1997
I
Isoprene synthase
Populus canescence
Schnitzler et al., 2005
J
Geranyl pyrophosphate
synthase
Antirrhinum majus
Tholl et al., 2004
K
Monoterpene synthase
Clarkia breweri
Pichersky et al., 1995
L
Geranyl geranyl
pyrophosphate synthase
Antirrhinum majus /
Nicotiana tabacum
Orlova et al., 2009
M
Phytoene synthase
Capsicum annuum
Dogbo et al., 1988
Notes S2 Trait and isoprene database
A database of isoprene and monoterpene emissions was compiled from the published literature. We
began
with
the
online
database
published
by
Wiedinmeyer
et
al.
(2004)
(http://bai.acd.ucar.edu/Data/BVOC/). This was used as a primary source of published emission
literature only. All primary emission and trait data were independently extracted from the original
literature.
We then used systematic searches to locate additional isoprene and monoterpene
emissions data, focusing on publications since 2004. The conditions under which the emission data
were collected were recorded (e.g. cuvette temperature, light, plant part measured, plant age, leaf
age, canopy position, growing conditions, measurement technique). All emission data were
converted to standardised values (µg g-1 h-1) using the Guenther equation (Guenther et al., 1993).
Emission data were then classified according to data quality. For the analyses reported here, only
emission data that were derived from measurements taken from upper canopy or “sun” (nonshaded) leaves of mature field-grown plants, sampled under non-droughted conditions, were used.
The emission data used in Fig. 2 were derived from Arey et al., 1991; Winer et al., 1992; Tanner &
Zielinska, 1994; Arey et al., 1995; Konig et al., 1995; Guenther et al., 1996a,b; Kempf et al., 1996;
Kesselmeier et al., 1996, Street et al., 1996; Cao et al., 1997; Owen et al., 1997; Street et al.,
1997a; Hakola et al., 1998; Owen et al., 1998; Guenther et al., 1999; Janson et al., 1999; Owen &
Hewitt, 2000; Boissard et al., 2001; Hakola et al., 2001; Harrison et al., 2001; Janson & de Serves,
2001; Owen et al., 2001; Owen et al., 2002; Greenberg et al., 2003; Moukhtar et al., 2005; Geron et
al., 2006a; Grabmer et al., 2006; Dominguez-Taylor et al., 2007; Llusia et al., 2008; Llusia et al.,
2009; Winters et al., 2009; Jardine et al., 2010 and Rinnen et al., 2011. Although extremely low
emission rates are occasionally reported, it is generally assumed that these are below the detection
limit of most analytical systems and therefore erroneous. We have adopted a conservative lower
limit (0.6 g/g/h) as the cut-off for distinguishing between emitters and non-emitters.
Data for Fig. 3 were derived from references Lamb et al., 1986; Ohta, 1986; Arey et al., 1991;
Winer et al., 1992; Tanner & Zielinska, 1994; Arey et al., 1995; Fuentes et al., 1995; Pier, 1995;
Guenther et al., 1996a,b; Harley et al., 1996; Kempf et al., 1996; Kesselmeier et al., 1996; Street et
al., 1996; Geron et al., 1997; Hansen et al., 1997; Harley et al., 1997; Owen et al., 1997; Pier &
McDuffie, 1997; Street et al., 1997a; Hakola et al., 1998; Owen et al., 1998; Guenther et al., 1999;
Isebrands et al., 1999; Janson et al., 1999; Anderson et al., 2000; Lerdau & Throop, 2000; Zhang et
al., 2000; Geron et al., 2001; Janson & de Serves, 2001; Owen et al., 2001; Geron et al., 2002;
Otter et al., 2002; Owen & Hewitt, 2000; Greenberg et al., 2003; Harley et al., 2003; Geron et al.,
2006b; Grabmer et al., 2006; Tambunan et al., 2006; Llusia et al., 2008; Winters et al., 2009;
Niinemets et al., 2010 and Rinnan et al., 2011.
Trait data (shade tolerance, photosynthetic capacity (Amass nmol g-1 s-1), specific leaf area, leaf
lifespan) were then added to the database. Specific leaf area (SLA) data were sourced only from
publications used for the emissions database. Data for the shade tolerance index were taken from
Niinemets & Valladares, 2006). This index, which runs from 1 (least shade tolerant) to 5 (most
shade tolerant), was derived from a large number of region-specific shade tolerance classifications
that were carefully calibrated against one another to form a composite index (details in Niinemets &
Valladares, 2006).
Data for photosynthetic capacity and leaf lifespan were drawn from the literature, aggregated to
species-mean values, and matched to the isoprene emissions data. If photosynthesis data were
reported in VOC emissions papers these were used in preference to the data derived from literature
searches. The “Glopnet” data compilation (Wright et al., 2004) was the primary source of additional
trait data, supplemented with data from Gower et al., 1993; Abrams & Mostoller, 1995; DeLucia &
Thomas, 2000; Kazda et al., 2000; Nagel et al., 2002; Turnbull et al., 2002; Mediavilla & Escudero,
2003a,b; Gratani & Varone, 2004; Holscher et al., 2004; Juhrbandt et al., 2004; Midgley et al.,
2004; Silla & Escudero, 2004; Cavender-Bares et al., 2005; Springer et al., 2005; Gratani &
Varone, 2006; Holscher et al., 2006; Negi, 2006; Funk & Vitousek, 2007; Kayama et al., 2007;
Santiago & Wright, 2007; Zheng & Shangguan, 2007 and IJ Wright (unpublished data).
Notes S3 Experimental and field evidence for seasonal leads and lags between isoprene
emission and photosynthesis
We have compiled information from the literature (Table S2) on seasonal differences in timing of
isoprene emission with respect to photosynthesis and leaf age. The approaches to defining leads and
lags differ between studies, and it is therefore not possible to standardise these reports.
Table S2 Observational or experimental evidence for lag in emissions
Study organism
Mucuna sp.
(Velvet bean)
Plant functional type
Legume
Observations
Lab measurements,
with isoprene
measured on leaf
discs after net
assimilation
measurements made
BVOC
isoprene
Results
Photosynthesis increases immediately;
isoprene only starts to increase after day 4;
both peak simultaneously, and then both
drop; significant isoprene production occurs
only after development of photosynthetic
competence; isoprene decreases before
photosynthesis decreases.
Reference
Grinspoon et al.,
1991
Mucuna sp.
(Velvet bean)
Legume
Lab measurements of
net assimilation and
isoprene emission
under low and high
light for 12-14 days
isoprene
Under low light, maximum photosynthesis
reached by day 4, but maximum isoprene
emission not reached until day 12; under high
light, photosynthesis increases linearly, but
isoprene emission increases with a rising rate
of increase, both reach maximum on day 14;
significant isoprene production occurs only
after development of photosynthetic
competence.
Grinspoon et al.,
1991
Mucuna sp.
(Velvet bean)
Legume
isoprene
Emission started on day 4 after budburst, and
was closely correlated with isoprene synthase
activity; 100-fold increases in emission rate
and enzyme activity occurred from leaf
emergence to 14 days
Kuzma & Fall, 1993
Pueraria lobata
(Kudzu)
Vine
Pot experiments, with
supplemental lighting
and varying
temperatures; leaf age
measured by tagging
from budburst;
isoprene measured on
leaf discs after net
assimilation
measurements made
Growth chamber
experiments; isoprene
and photosynthesis
were measured under
standard conditions of
isoprene
No measurements made of isoprene until
leaves reached full size; at full size
photosynthesis 50% of maximum but no
isoprene emission detected; isoprene
emission detected ca 1 week after full
Sharkey & Loretto,
1993
1000gmol
photons m2 s-1 and
30C; isoprene
measured by gas
chromatography of
cuvette samples
Growth chamber
experiments; standard
light and temperature
conditions (30C and
1000 mmol m-2 s-1);
isoprene measured
using reduction gas
detector; leaf age
indexed by area
Leaf measurements in
situ; pot experiments
at different
temperatures;
photosynthesis
measured using
LiCOR; isoprene on
cuvette samples by
gas chromatography
expansion
Mucuna sp.
(Velvet bean)
legume
Isoprene
Onset of positive rates of net photosynthesis
precedes that of isoprene emission by 3-4
days, and reached only 50% of maximum rate
by day 5-7. During leaf senescence,
photosynthesis rate and isoprene emission
rate declined in parallel
Harley et al., 1994
Populus
tremuloides
Deciduous broadleaf tree
Isoprene
Onset of isoprene emission was delayed for
up to 4 weeks after bud burst, despite positive
net photosynthesis rates. Maximum isoprene
emission rates were reached ca 6 weeks after
leaf emergence. Onset of emissions begins
after ca 400 degree days (GDD5).
In the pot experiments, leaves that emerged
under cool, springtime temperatures did not
emit isoprene until 23 days after bud burst,
whereas leaves that emerged in hot,
midsummer temperatures emitted isoprene
within 6 days.
In P. deltoides and P. vulgaris, methanol
emission declines with increasing leaf age
after leaf expansion, consistent with
volatilization from a cellular pool that
declines in older leaves. But in Glycine max,
it initially increases and then decreases. All
continue to emit even from senescent leaves.
Leaves emerge day 140 and fully developed
by day 160; onset of senescence day 240;
photosynthesis ceased by day 290; first
Monson et al., 1994
Populus deltoides
var occidentalis;
Glycine max and
Phaseolus
vulgaris
Temperate deciduous
broadleaf tree; legume;
legume
Pot experiments;
Methanol measured
using enzymatic
fixation; PAR by
LiCOR
methanol
oak (mostly red),
red maple, red
pine, hemlock
Temperate deciduous
broadleaf trees (Harvard
Forest)
Isoprene measured by
flux-gradient
similarity approach;
isoprene
Nemecek-Marshall
et al., 1995
Goldstein et al.,
1998
birch, white pine,
and cherry
LAI estimated from
measurements of
PAR
Deciduous
broadleaf forest
(Populus
tremuloides,
Populus
grandidentata)
Deciduous broadleaf tree
Field LiCOR
measurements of LAI
and isoprene
measured on air
samples by gas
chromatography
isoprene
Boreal aspen
forest (Populus
tremuloides) with
<8% Populus
balsamifera,
Picea glauca, and
Picea mariana
Deciduous broadleaf tree
Field LiCOR
measurements of LAI
and isoprene
measured on air
samples by gas
chromatography
isoprene
Quercus
macrocarpa
Growth chamber
experiments on young
trees, with varying
controlled
temperatures (20-
isoprene emissions detected day 152, when
temperature > 25C. Isoprene emissions
decreased after day 250, coinciding with
decreased air temperature, nighttime
temperatures falling below 10ºC regularly,
photosynthetic uptake by the canopy
declining, and leaf senescence. Normalized
rates at 30C and 1000 mmol m-2 s-1
The seasonal course of the normalized
emission rate reached its peak 4 weeks after
leaf out and 2 weeks after emissions began;
the normalized rate remained relatively
constant between days 165 to 230, and
decreased steadily after day 230 as the leaves
senesced reaching zero by day 300.
Isoprene emissions started 2 weeks after
maximum leaf expansion (GDD threshold of
390) and maximum emissions 4 weeks after
maximum leaf expansion; slow increase tied
to low temperature. Decline in isoprene
occurred 10 days after visual observation of
onset of leaf senescence
Budburst day 120, full leaf-out by 150,
senescence started day 200; isoprene at
background level until day 150 although
temperatures on some days were > 15ºC. (NB
Says “2 weeks delay” in text, but estimate
here is from Figure). Maximum isoprene
emissions day 200-210, but this interval also
includes days with low temperatures and
therefore low emissions; isoprene emission
continued through senescence period
Isoprene emission started 11-12 days after
budburst, after 187-204 degree days (GGD0);
The GDD between bud-break and the first
day of maximum isoprene emission ranged
from 528 to 885 and occurred 3 to 5 weeks
Fuentes & Wang,
1999
Fuentes et al., 1999
Petron et al., 2001
Quercus ilex
Evergreen broadleaf tree
Populus
x
euroamericana
Deciduous broadleaf tree
Hymenaea
courbaril
Drought-deciduous tropical
broadleaf tree (leaf
exchanger)
Populus
grandidentata,
Quercus rubra
Temperate deciduous
broadleaf tree
30C); photosynthesis
and isoprene
measured using an
open-path gas
exchange system with
a temperaturecontrolled leaf cuvette
Field measurements
of emission using a
cuvette system
FACE experiment,
with elevated CO2
(550 mmol mol-1),
and nutrient
treatment;
measurements at
standard light and
temperature (1000
mmol m-2 s-1) (30C)
Branch enclosure
sampling in situ; PAR
measured using
LiCOR outside
chamber; BVOCs
measured by gas
chromatography
Eddy covariance
measurements during
growing seasons,
1999-2002
after bud burst.
monoterpenes
isoprene
isoprene
Emissions started ca 4 weeks after budburst
and peaked late August/early September;
emissions decline in autumn (prior to
abscission in year-old leaves) and were
minimal in current year leaves in winter
Leaf development on a single plant (assessed
by leaf area); no detectable emission on leaf
2, but emitting by leaf 3 (42% of full area);
isoprene emission highest on leaves 15 and
16 and declined in older leaves; decline faster
under ambient CO2
Fischbach et al.,
2002
No delay in emission on budburst because
temperatures were high. Highest emissions
found for young mature leaves in the dry
season (28–29 days after bud burst). Decline
in emission for older mature leaves in the wet
season (226–227 days after bud burst).
Lowest emissions found for senescent leaves,
because of breakdown of metabolic activity
and loss of leaf nitrogen.
Isoprene emission from Populus
grandidentata occurred between 23-33 days
after bud burst; isoprene emission from
Quercus rubra occurred 23-36 days after bud
burst (cumulative average daily temperature
since the last spring frost, HDD = 437–507).
In 2002, the last spring frost was ca 1 month
Kuhn et al., 2004
Centritto et al.,
2004
Pressley et al., 2005
Pueraria lobata
(Kudzu)
Pinus ponderosa
Evergreen needleaf tree
Populus alba
Deciduous broadleaf tree
Populus tremula
Deciduous broadleaf tree
Temperature
controlled greenhouse
experiments, 20 and
30C; isoprene
measured by gas
chromatography on
cuvette samples;
measurements under
standard conditions
(30C and 1000 mmol
m-2 s-1).
Above canopy
measurements of
isoprene through
seasonal cycle
FACE experiment
(high and ambient
CO2); measurements
made at ambient
temperature (30–35
°C) and light intensity
(> 1500 mmol
photons m-2 s-1) and
at controlled leaf
temperature (25 or 35
°C); respiration
measured by LiCOR,
isoprene by gas
chromatography; leaf
age by degree of
expansion
PTR-MS
measurements on cut
branches in laboratory
later and emission occurred 26–31 days
afterwards at approximately 406 HDD.
Kudzu grown at 30C emits isoprene at least
a week before leaves fully expanded and 1
day after becoming photosynthetically
competent. When grown at 20C, leaves did
not emit isoprene until 1 week after they
became fully expanded and 2 weeks after the
onset of photosynthetic competence.
Wiberley et al.,
2005
monoterpene
Monoterpene emissions highest in spring and
winter (i.e. in young and old leaves) and
minimal in summer.
Holzinger et al.,
2006
isoprene
Low emission rate of isoprene in the leaf that
was not completely expanded, compared with
fully expanded leaves both when sampled at
25 and 35 °C. Isoprene emission inversely
related with respiration rate in younger leaves
(though not older leaves) because high rates
of respiration requires carbon that would
otherwise be allocated to isoprene
biosynthesis.
Loretto et al., 2007
isoprene
Percentage of carbon lost due to isoprene
emission gradually increased during leaf
senescence. Isoprene emissions were present
even in leaves just before abscission.
Sun et al., 2012
Notes S4 Analysis of isoprene emissions at a regional scale
The relationship between the seasonality of photosynthesis and emission of isoprenoids was
investigated by comparing the seasonal cycles of remotely sensed formaldehyde (HCHO) total
column with Leaf Area Index (LAI). Formaldehyde is mostly produced by oxidation of volatile
isoprenoids and can be used to estimate or constrain the emission of isoprene and other BVOCs
(e.g. Shim et al., 2005; Palmer et al., 2003, 2006; Fu et al., 2007; Barkley et al., 2008, 2011; Foster
et al., subm). We focus on two areas with vegetation types dominated by summergreen or raingreen
broadleaf deciduous trees, i.e. where broadleaf and deciduous vegetation covers at least 30% and
evergreen vegetation covers < 1% of the surface according to MODIS remotely sensed vegetation
continuous fields (Defries & Hansen, 2009). The HCHO data (Level-2 OMI Formaldehyde Data
Product, V3: Chance, 2002; Kurosu, 2004) are based on measurements using the Ozone Monitoring
Instrument (OMI) using a retrieval algorithm that is based on non-linear least-squares fitting. Fitting
uncertainties for the HCHO slant columns (single measurement) typically range between 40 and
100%, with the lower end of this range over HCHO hotspots. OMI has a 13 by 24 km2 spatial
resolution at nadir and achieves global coverage daily; we average the data on to the 2º x 2º grid
over 8-day periods. LAI was obtained from Collection 4 of the Terra and Aqua Moderate
Resolution Imaging Spectroradiometers (MODIS) LAI product (Yang et al., 2006). This product
has a 1 km resolution and an 8-day time resolution. The HCHO column data can also reflect
emissions from biomass burning. We therefore include active fire counts processed from the
MODIS/TERRA data by Giglio et al., 2006 for comparison. The air temperature at 2 m is derived
from GEOS-5 (Rienecker, 2008). The data are all rescaled to a 2º by 2º grid cell size. At this
resolution, it is expected that about 50% of the isoprene produced within a grid cell is oxidised to
formaldehyde inside that grid cell. Formaldehyde and 2 m air temperature have been smoothed with
a 56-day running mean.
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