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ANNUAL
REVIEWS Further Cellulosic Biofuels
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Andrew Carroll1 and Chris Somerville2
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• Top cited articles email: andrew.carroll@berkeley.edu
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Annu. Rev. Plant Biol. 2009. 60:165–82 Key Words

First published online as a Review in Advance on cellulose, lignocellulose, biomass, bioenergy, fuels
November 17, 2008

The Annual Review of Plant Biology is online at Abstract

plant.annualreviews.org
The development of sustainable, low-carbon, liquid fuels from cellulosic
This article’s doi: biomass will require advances in many areas of science and engineering.
10.1146/annurev.arplant.043008.092125
This review describes the major topics of enquiry concerning cellulosic
Copyright  c 2009 by Annual Reviews. biofuels with an emphasis on those areas of research and development
All rights reserved
that include research problems of interest to plant biologists.
1543-5008/09/0602-0165$20.00

165
 ANRV375-PP60-08 ARI 25 March 2009 13:17
Contents
INTRODUCTION . . . . . . . . . . . . . . . . . .
THERMAL CONVERSION
TECHNOLOGIES . . . . . . . . . . . . . . .
BIOCONVERSION
PRETREATMENT
AND HYDROLYSIS . . . . . . . . . . . . . .
MICROBIAL CONVERSION
OF SUGARS TO FUELS . . . . . . . . .
CHEMICAL CONVERSION
OF SUGARS TO FUELS . . . . . . . . .
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POTENTIALLY USEFUL
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GENETIC MODIFICATIONS . . .
ENVIRONMENTAL ASPECTS . . . . .
CHOICE OF SPECIES . . . . . . . . . . . . . .
WOODY SPECIES . . . . . . . . . . . . . . . . . .
AGRONOMIC ASPECTS . . . . . . . . . . .
THE CHALLENGE OF
MARGINAL LANDS . . . . . . . . . . . . .
HOW MUCH FUEL COULD
BE PRODUCED? . . . . . . . . . . . . . . . . .
CONCLUDING REMARKS . . . . . . . . .
INTRODUCTION
Many scientists are convinced that the most
pressing single problem facing humanity is cli-
mate change resulting from the anthropogenic
loading of greenhouse gasses such as CO2 ,
N2 O, and methane into the atmosphere (51).
A major fraction of CO2 emissions arise from
burning fossil fuels, which supply approxi-
mately 85% of energy consumption. In con-
sidering the ways in which energy production
can be decarbonized, one is inexorably drawn
to the fact that the surface of the earth receives
approximately 9000 times as much energy from
the sun as all human energy uses (59). Energy
from the sun is being used to produce power
or fuels in four ways: via wind turbines to gen-
erate electricity, by photovoltaic conversion to
electricity, by using mirrors to heat sterling en-
gines that ultimately produce electricity, and by
harvesting plant biomass that can be burned as
solid or liquid fuels. A fifth possibility, the pho-
166 Carroll · Somerville
toelectrochemical production of hydrogen, is
promising but needs substantial further devel-
opment. At present, none of these approaches
166
represent a clear solution to our energy needs.
Thus, it is essential to approach energy produc-
166
tion through a basket of complementary tech-
nologies rather than to rely on a single tech-
nology. Because biomass is currently the most
168
cost-effective route from photons to fuels (as
opposed to power), much of the emphasis in
169
the biofuels area has been focused on the uses of
biomass for that purpose. Additionally, biomass
169
replacing fossil fuel for transportation uses is
attractive in that it is more difficult to capture
170
CO2 emissions from transportation uses than
172
other types of energy use because of the highly
173
distributed use.
175
Although liquid biofuels are currently made
175
almost entirely from sugar, starch, or fats and
oils, we believe that the use of food for fuel is
176
not sustainable in the face of expanding de-
mand for food, feed, and fiber and that the
177
long-term opportunity to produce fuels from
177
biomass will be largely restricted to using lig-
nocellulose and possibly algal lipids or ter-
penes. In this review we summarize some of the
issues associated with the development of cel-
lulosic transportation fuels and outline some of
the scientific questions in plant biology that are
related specifically to this topic. Many other re-
views of this subject and related matters have
appeared recently (40, 53, 60, 77, 86, 88).
THERMAL CONVERSION
TECHNOLOGIES
Several different technologies exist for conver-
sion of lignocellulose to fuels and the choice
of technology can have substantial implications
for environmental and agronomic aspects of
biofuels production. Perhaps the simplest tech-
nology is to burn biomass to produce steam
that can be used to drive electricity genera-
tion. In principle, this technology can produce
greenhouse gas benefits by displacing coal, the
main source of fuel for electricity generation.
Biomass is used for electricity generation in in-
dustries such as the pulp and paper industry
 ANRV375-PP60-08 ARI 25 March 2009 13:17
or the sugarcane processing industry where
biomass is readily available and specialized fur-
naces are used (68). The main limitation to the
widespread use of biomass for this purpose at
present is that coal-fired plants are generally
very large to take advantage of economies of
scale, so it is not feasible to accumulate enough
biomass to supply many existing plants at prices
comparable to coal because of transportation
costs of low energy density biomass. Addition-
ally, coal-fired plants use finely pulverized coal
dust (∼100 um particles) that burns with very
high efficiency. Because of the fibrous nature of
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biomass, it is relatively expensive to grind it to
very small particles, so inclusion of biomass at
more than approximately 10% of total mass de-
creases the efficiency of coal combustion. Some
types of biomass are also high in minerals such
as potassium and silica that create ash or foul
the furnaces. It would be interesting, in this re-
spect, to develop varieties of high-silica species,
such as rice (95), that have reduced levels of sil-
ica. If reduction of silica does not have adverse
effects on yield, the development of silica-free
varieties could facilitate the use of agricultural
residues from such varieties.
A related technology is thermal conversion
of biomass to syngas, a mixture of CO2 , CO,
CH4 , N2 , and H2 . When biomass (or fossil
fuel) is heated to approximately 800–900◦ C,
the organic molecules that comprise biomass
rapidly decompose to syngas plus some resid-
ual char and tar. The syngas can be con-
verted by specialized catalysts to a wide vari-
ety of other molecules that include methanol,
ethanol, and dimethyl ether (DME), as well
as a variety of hydrocarbons and waxes that
can be reformed to fuels that resemble gaso-
line and diesel (47). Methanol can be converted
efficiently to gasoline by a catalyst that has
been used industrially to make gasoline from
methane via methanol (the Mobile process).
Unlike methanol or ethanol, DME is compati-
ble with blending in diesel fuel and is considered
an attractive fuel.
The attractive aspect of the syngas route to
fuels is that the method is relatively insensitive
to the composition of biomass compared with
bioconversion technologies. Thus, in principle,
processing facilities could use different materi-
als throughout the year depending on availabil-
ity. Additionally, syngas can be produced from
nonbiomass materials such as plastics. In this re-
spect, this method is well suited for conversion
of urban waste to fuels. Furthermore, because
the methods were developed to utilize coal, it is
possible to envision facilities that use both coal
and biomass (or urban waste) to obtain econ-
omy of scale or to modify the composition of
the syngas. The constituents of biomass also
undergo chemical transformations to bio-oils
or gases (e.g., methane) in supercritical water
at high temperature and pressure (74). This ap-
proach has been suggested to be more energy
efficient because it operates at lower tempera-
tures and avoids a water-to-steam phase transi-
tion. However, the product mix is complex and
additional work is needed to assess the overall
efficiency compared with syngas.
The challenges associated with the syngas
route include that the fuel synthesis reactions
take place at high temperature and pressure us-
ing catalysts that may be poisoned or fouled
by components of biomass. The costs of build-
ing reactors generally decrease as a function
of size, thereby favoring construction of large
facilities. Large size is not necessarily a prob-
lem for coal-based facilities because coal can be
transported at low cost from a mine to a facil-
ity. By contrast, biomass is distributed and less
dense than coal so the cost of collection and
transport to a central facility is higher. Thus,
to minimize transport costs, biomass conver-
sion facilities are expected to be relatively small
(50–150 Mgal/year) compared with coal gasi-
fication plants or coal-fired power generat-
ing plants. The process results in a substantial
change in entropy so that approximately half
of the energy present in biomass is dissipated
during the process.
An important variant of syngas technology
involves a reaction called the gas water shift in
which oxygen from water combines with CO to
produce CO2 and H2 . The highly condensed
streams of CO2 and H2 can be separated and
the highly enriched CO2 can be compressed
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for geological sequestration (57). The H2 can be
burned directly in a gas turbine to produce elec-
tricity, compressed for use in fuel cells, or used
to upgrade biomass (or fossil fuels) to higher
quality liquid fuels (12, 46). Another variant is
fast pyrolysis, a method in which biomass is
heated at a rate of approximately 500◦ C/s to
temperatures of 400–600◦ C, which causes de-
composition of biomass to a mixture of approx-
imately 300 compounds, then rapidly cooled to
quench the reactivity of the mixture. Passing
the pyrolysis products through certain catalysts
results in production of a high proportion of
aromatic compounds that can be blended di-
rectly with gasoline (7). Because the engineer-
ing costs associated with pyrolysis are expected
to be much less than with production of fu-
els from syngas, further improvements in this
area may allow the development of small-scale
biomass-to-fuel conversion facilities.
In addition to chemical conversion of syn-
gas to fuels, it is possible to produce ethanol,
butanol, and other fuels by bioconversion of
syngas using a number of bacterial species (42).
Bioconversion may have some advantages such
as lower sensitivity to catalyst poisoning and
flexibility in regard to the composition of the
syngas. However, the low aqueous solubility of
syngas creates challenges associated with ob-
taining adequate mass transfer of syngas to the
cells.
BIOCONVERSION
PRETREATMENT
AND HYDROLYSIS
The potential attractiveness of bioconversion
technologies for liquid fuel production is re-
lated to the idea that bioconversion technolo-
gies are relatively scale-neutral and may have
lower capital costs than thermal conversion
methods. Thus, bioprocessing facilities are gen-
erally envisioned to be scaled so that biomass
transportation costs are a small fraction of total
fuel production costs. Additionally, it is gener-
ally believed that technical innovations may re-
duce the capital costs of producing cellulosic fu-
els to the point that farmers’ cooperatives have
168 Carroll · Somerville
the financial resources to participate in owner-
ship of the facilities, as is currently the case for
many of the grain ethanol production facilities
in the United States.
The key steps in bioconversion of lignocel-
lulose to fuels are size reduction, pretreatment,
hydrolysis, and fuel production (44). Size reduc-
tion is accomplished by mechanically cutting
biomass to facilitate access of reagents to the
lignocellulose. For woody species, it has been
estimated that size reduction to submillimeter
scale could consume a few percent of the en-
ergy in the cellulosic ethanol produced using
current technology. In one study, size reduc-
tion of hardwood to 1.6 mm particles required
130 kwh/metric ton (t) versus 7.5 kwh/t for
straw (6). In addition to optimization of me-
chanical processing to reduce energy, the only
other way of reducing this input cost seems to
be in developing reagents for hydrolysis that ei-
ther penetrate biomass and can decompose the
material from within or are highly active on the
surface of biomass particles. Measurements of
wheat internode cell wall porosity suggest that
most spaces within the walls are less than 3 nm
in diameter (11). Because the stokes radius of a
20-kD protein is approximately 2.5 nm, the im-
plication is that to penetrate biomass, enzymes
or other catalysts must be less than approxi-
mately 20 kD in size, which would be on the
low side for most hydrolytic enzymes.
The role of pretreatment methods is to in-
crease the porosity of biomass particles and
to increase the accessibility of cellulose and
other polysaccharides to enzymes (94). How-
ever, most pretreatment methods also result in
some hydrolysis. The most widely used method
involves heating in dilute acid such as 0.9%
H2 SO4 . Treatment for a little as one minute at
180◦ C in 0.9% H2 SO4 can result in solubliza-
tion of as much as 90% of the xylan (25). The
solublization is presumably associated with two
types of chemical reactions: (a) the hydrolysis of
xylans to sugars and oligosaccharides with much
higher solubility than intact xylans and (b) the
hydrolysis of lignin-xylan or xylan-xylan esters
and of acetyl groups on polysaccharides (32).
Because a substantial amount of xylan is thought
 ANRV375-PP60-08 ARI 25 March 2009 13:17
to be hydrogen bonded to the surface of cellu-
lose microfibrils, the acid pretreatment presum-
ably exposes the cellulose microfibrils to some
extent, both by hydrolysis of xylan and also by
releasing lignin from indirect association with
cellulose via linkage to xylan. Other methods,
such as ammonia fiber expansion, cause similar
effects (94).
Following pretreatment, solubilized sugars
are separated from solids and the solids are sub-
jected to further hydrolysis (43). At present, the
second round of hydrolysis is catalyzed by en-
zymes that can collectively hydrolyze cellulose
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and hemicellulose to free sugars, although there
is interest in the possibility of using synthetic
catalysts instead of enzymes. Relatively large
amounts of enzyme (e.g., ∼25 kg/ton of cel-
lulose) are reportedly required to release most
of the sugars from biomass at rates compatible
with high-throughput processes (44). The re-
quirement for unusually large amounts of en-
zymes appears to be the single largest cost in
the production of cellulosic fuels from nonther-
mal routes. This cost has led to the search for
more active glycosyl hydrolases from incom-
pletely explored sources such as termites (93).
MICROBIAL CONVERSION
OF SUGARS TO FUELS
The principal components of plant cell wall
polysaccharides from most C4 grasses and trees
are glucose and xylose. Thus, a minimum ca-
pability of an industrial biofuel-producing mi-
croorganism is the ability to convert both of
these sugars to liquid fuel components such as
ethanol or other alcohols, alkanes, or terpenes.
Ultimately, the ability to use all sugars will be a
goal of industrial strain development. Although
the industrially adapted stains of yeast that are
used in the brewing industry cannot use xy-
lose, strains of yeast with this capability have
been developed through genetic engineering
(37), and many naturally occurring yeast and
bacteria have this capability.
In addition to using all sugars, microbial
strains must be resistant to the compounds pro-
duced or released during biomass degradation
(44, 75). Because it is desirable to have concen-
trated sugar solutions to minimize volume and
minimize dilution of product, the biomass hy-
drolyzate usually has high solids loading (e.g.,
>20% solids is desirable) and therefore may
contain relatively high concentrations of toxic
compounds. Thus, for instance, acid pretreat-
ment of biomass produces dehydrated sugars
such as furfural and hydroxymethyl-furfural
that are toxic to yeast (75, 76), and some poten-
tial biomass crops contain secondary metabo-
lites that are toxic to microorganisms. Identifi-
cation and elimination of such compounds by
genetic methods is a priority for research on
plant feedstocks if it can be done without cre-
ating pest and pathogen problems.
CHEMICAL CONVERSION
OF SUGARS TO FUELS
A new thrust in research on biomass conversion
is the use of synthetic catalysts to convert sugars
to fuels such as alkanes by what is called solution
phase reforming (46, 47). As with bioconver-
sion, reforming starts with sugars, which are de-
hydrated, condensed, and reduced to produce
alkanes or other hydrophobic compounds. The
formation of alkanes requires hydrogen, which
may be obtained from the sugars or from an
external source. If externally provided hydro-
gen is used, no carbon is lost from the biomass
during the conversion and, in effect, biomass-
derived carbon would become a carrier for hy-
drogen. Thus, if hydrogen becomes available
in large amounts from some low-carbon source
such as electrolysis, direct photoelectrolysis, or
fossil fuel reforming accompanied by geologi-
cal sequestration (57), this type of conversion
might be an attractive way to introduce hy-
drogen into the existing fuel economy. Biofuels
made this way would require several-fold less
land than cellulosic ethanol per unit of fuel and
would not have the infrastructure issues asso-
ciated with ethanol. In particular, most of the
several hundred million vehicles in the United
States are not designed to use fuels contain-
ing more than 10% ethanol (E10). This fact is
expected to limit use of ethanol in the United
www.annualreviews.org • Cellulosic Biofuels 169
 ANRV375-PP60-08 ARI 25 March 2009 13:17

States to approximately 15 billion gallons per

year.

Cellulose
In addition to the challenge of develop-

39.01
37.69
32.64

39.23
48.07
30.97
33.08
34.01
41.7
ing inexpensive and effective methods of hy-
drolyzing biomass to sugars, implementation of
synthetic catalysts will require substantial re-
search into the effects of biomass composition

Galactan
0.46
0.87
0.75

0.88
0.74
0.92
1.04
0.52
on the reforming process and the catalysts. Be-

2.4
cause many catalysts are inactivated by com-
pounds that are abundant in biomass, it may
be necessary to develop methods for refining

Mann
0.35
0.38
0.31

1.81
1.23
0.29
0.27
biomass-derived sugar streams to remove cat-

10.7

0.2
alyst poisons. Alternatively, Mascal & Nikitin
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(62) recently reported the direct acid-catalyzed

conversion of cellulose to diesel-compatible fu-

Xylan
22.05
21.61
19.22

13.07
10.42
20.42
20.93
14.14
5.9
els by a method that seems likely to be insensi-
tive to inhibitors.

Arabinan
2.06
2.42
2.35

0.89

2.75
3.01
1.65
POTENTIALLY USEFUL

1.6

0.3
GENETIC MODIFICATIONS
The major components of plant secondary cell

No data
walls are cellulose, hemicellulose, and lignin
Uronic
Acids
2.16
2.99
2.24

4.31
4.07
1.17

1.07
2.5
(38). The amount of lignin is not of concern
if biomass is to be converted to fuels through
a thermal process. By contrast, the rate of en-
zymatic hydrolysis of cellulose to sugars is in-
Lignin
23.09
18.59
16.85

25.18
26.91
17.56
17.54
16.09
25.9
versely proportional to the amount of lignin
present in biomass, and a difference of a few
Table 1 Composition of some prospective energy crops1

percentage points in lignin content has a large

effect on the efficiency of cellulose digestion
3.66
10.06
10.22

2.03
1.22
5.76
6.42
5.04
Ash

0.3

(9). A feedstock with a lignin content of 22%

was predicted to yield only half the sugar of a
feedstock with 17% content, and a feedstock
Extractives

with 26% lignin content would yield almost no

3.78
5.61
12.95

6.89
4.15
16.99

22.03
2.7

13.8

sugar. Thus, by this criterion, herbaceous crops

are better suited for bioconversion than woody
crops (Table 1). The percentage lignin content
of bamboo (25%), poplar (22%), and sugarcane
bagasse (26%) are substantially higher than
Switchgrass (cave-in-rock)

that of switchgrass (17%), Miscanthus (17%),

Switchgrass (alamo)

and alfalfa (17%) (24, 62). However, modest

Sugarcane bagasse

changes in lignin composition may be engi-

Sweet sorghum
Monterey pine
Hybrid poplar
Wheat straw

neered (92). For instance, transgenic poplar

Corn stover

Eucalyptus

(45) and alfalfa (10) have been produced with

Source

reduced lignin accumulation. These plants have

reduced lignin content: from 17.6% to ∼14%
in alfalfa and from 20.6% to 12.8% in poplar.

170 Carroll · Somerville

 ANRV375-PP60-08 ARI 25 March 2009 13:17
Progress in breeding for useful variation in cell
wall composition is also possible (79).
Modification of lignin composition rather
than amount is also useful. Transgenic poplar
trees in which ferulate 5-hydroxylase expres-
sion was increased had increased ratios of sy-
ringyl to guaiacyl moieties (49). Wood from the
modified trees required 60% less Kraft pulping
time than controls, a very significant improve-
ment in energy and process residence time.
This effect may be due to a reduced degree of
branching of syringyl lignin (35). In principle,
it may also be possible to reduce the degree of
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ferulate-mediated cross-linking of arabinoxy-
lans to themselves and to lignin. However,
at present the enzymes that catalyze forma-
tion of ferulate esters to hemicellulose are not
known (4, 35), and the functional importance
of cross-linking has not been studied in intact
plants.
A conceptually important idea about lignin
modification is to engineer plants to secrete
compounds that could become incorporated
into lignin but could be more readily cleaved
than lignin because of the presence of an appro-
priately placed linkage such as an ester or amide
(78). This idea builds on the fact that lignin is
formed through a free radical process that can
accommodate substantial structural diversity in
the precursors. The key factor is probably the
substrate specificity of the peroxidases that are
thought to catalyze oxidation of lignin precur-
sors. The challenge in creating a readily cleaved
lignin would be to identify a pathway for the
synthesis of a suitable precursor.
Cell wall polysaccharides are acetylated to
varying degrees (70, 73). Pretreatments hy-
drolyze these esters, releasing acetate, which
is inhibitory to microorganisms. The role of
polysaccharide acetylation is not understood.
Presumably the addition of acetyl groups re-
duces the solubility of polysaccharides and
thereby favors the deposition of a highly insolu-
ble cell wall. However, it would be interesting to
explore the degree to which acetylation could
be genetically reduced in plant tissues to de-
crease the production of inhibitory compounds
during cell wall decomposition.
One of the most challenging aspects of
making cellulosic fuels is hydrolysis of cellu-
lose. Even after the lignin and hemicellulose
that are thought to coat cellulose microfibrils
are dislodged or degraded, the cellulose mi-
crofibrils remain recalcitrant to hydrolysis by
cellulases (43). The mechanistic basis of this
phenomenon may be related to the fact that
the cellulose microfibrils are rigid and large so
cellulases are sterically hindered from access-
ing the glycosidic linkages (69). Additionally,
endolytic cleavage does not necessarily lead to
dissociation of oligosaccharides from the mi-
crofibril because short glucans are insoluble and
are also hydrogen bonded to the microfibril.
Dissociation would be expected to decrease the
entropy of water that hydrates the glucans and is
therefore thermodynamically unfavorable (54).
Because of lack of knowledge about exactly how
microfibrils are made (87), it is not possible to
speculate about whether the structure of cellu-
lose can be altered in a useful way.
One approach to the apparent requirement
for large amounts of cellulase is to have the
plant make the cellulases. Experiments in which
cellulases and other hydrolytic enzymes were
expressed in transgenic plants have indicated
that it is possible to express hydrolytic enzymes
without causing damage to the plants under at
least some conditions (88). This is an interest-
ing approach that merits further investigation.
One of the possible problems is that the time
between biomass harvest and delivery to a pro-
cessing plant is expected to be up to a year or
more and the biomass is likely to be stored un-
der conditions of temperature extremes (i.e.,
bales under a tarp). Thus, the enzymes would
have to be quite robust.
Relatively little breeding has been done to
improve cell wall digestibility of any of the plant
species that are likely to be used for biofuels.
However, the available evidence indicates that
useful variation can be identified in genetically
divergent lines (82). Because it can be very ex-
pensive to carry out direct tests of digestibility,
there is a pressing need to identify the structural
features of cell walls and the morphological fea-
tures of plants that affect digestibility (83) and
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to develop high-throughput assays for those
features (63, 83).
ENVIRONMENTAL ASPECTS
A major driver of the development of cellulosic
biofuels is to produce low net carbon fuels in
a sustainable and environmentally benign man-
ner. To meet this general goal it will be neces-
sary to use crops and practices that minimize
emissions of nitrous oxide and fertilizer runoff
(22), do not deplete groundwater through irri-
gation (71), do not deplete soil carbon, and do
not stimulate biodiversity depletion or stimu-
late other problems such as proliferation of in-
vasive species or amplification of promiscuous
pests or pathogens.
One implication of these guidelines for en-
vironmental stewardship is that biofuel crops
should have high water use efficiency. Addi-
tionally, to utilize marginal lands, a high degree
of drought and salt tolerance may be advanta-
geous. In general terms, the demand for high
water use efficiency implies the use of C4 crops.
C4 plants concentrate CO2 in their leaves to
overcome the fact that oxygen competes with
CO2 as a substrate for Rubisco. The C4 process
is more efficient than C3 when carbon diox-
ide concentrations are low, temperatures are
high, or water is scarce (limiting gas exchange
through stomata) (1). The maximum theoreti-
cal efficiency for C4 plants (the percentage of
incident light converted into biomass) is 6% at
30◦ C with a CO2 concentration of 380 ppm;
this value is 4.6% for C3 plants. As the CO2
concentration increases over the next century,
C3 plants will gain parity at a CO2 concen-
tration of 700 ppm (96). However, in regions
where water is limiting, C4 plants are superior
because of high water use efficiency. As a result,
C4 plants are significantly more efficient in the
tropics and in temperate regions where water is
scarce. In cold and wet regions, C3 plants are
preferable. The majority of abandoned and de-
graded land is in tropical and/or dry locations
more favorable to C4 plants. However, a sub-
stantial amount of land will be more favorable
to C3 plants. Although development of C4 bio-
172 Carroll · Somerville
fuel crops will prove to be more significant, C3
biofuel plants will need to be developed to re-
alize the full potential of biofuels. Russia, for
example, has 20 Mha of abandoned land (50)
and 248 Mha of Siberian land that can be ex-
ploited without ecological damage (85). This
land would be more efficiently exploited by C3
plants adapted to the climate.
The requirement that biofuel crops not lead
to soil carbon depletion implies that biofuel
crops should be perennials or woody species. A
meta-analysis of the effect of crop cover on soil
carbon dynamics can be summarized as showing
that annual plowing causes release of soil carbon
relative to land planted with forest or pasture
(i.e., perennial grasses) (36). Perennial grasses
develop extensive root systems that in effect
transfer atmospheric carbon into soil biomass.
If the soil is not tilled and is protected from
erosion, the amount of biomass accumulating
in the soil can sequester a substantial amount
of carbon. A number of studies performed on
switchgrass have shown carbon sequestered in
the soil at annual rates of 1–10 t/ha (31, 65).
Significant variation in the values may reflect
that some studies have investigated the carbon
sequestration only at relatively shallow depths
(above 60–90 cm), whereas other studies that
probe deeper soil levels (up to 2 m) find that
the majority of carbon enrichment occurs at
lower depths. Perennials also control soil ero-
sion compared with annual crops (65). This fea-
ture of perennials may allow the use of sloping
land that is not suitable for annual crops. Simi-
larly, low land that remains too wet to till until
after the planting season may be suitable for
perennial energy crops.
The requirement for low nitrogen losses
also implies the use of perennial crops and
forest species and may favor certain nitrogen-
fixing species. The extensive root systems
associated with perennials are thought to min-
imize N losses to runoff (65). Also, because
much of the nitrous oxide emissions from field
crops take place before the crop has become es-
tablished and can take up fertilizer, the peren-
nials may have lower N2 O emissions because
they may take up applied nitrogen more rapidly
 ANRV375-PP60-08 ARI 25 March 2009 13:17
than annuals. The ability of some rhizomatous
species to mobilize mineral nutrients from the
aerial organs into the roots at the end of the
growing season may also reduce nitrogen emis-
sions. A species such as Miscanthus has a car-
bon to nitrogen ratio of about 700:1 at that
time (about 20 times lower than corn stover).
Depending on how the biomass is processed to
fuels, mineral nutrients may be recovered from
the residue for recycling to the land used to pro-
duce the biomass. This approach is used in sug-
arcane production where the stillage remaining
after fermentation and ethanol separation is dis-
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tributed onto sugarcane production land.
Industrial production of fixed nitrogen is a
major use of energy, accounting for almost 2%
of all human energy uses. Therefore, there is
interest in the idea that certain nitrogen-fixing
species may be useful.
CHOICE OF SPECIES
An important contribution that plant biologists
can make at present to the development of
cellulosic biofuels is to identify and charac-
terize plant species that may be useful bioen-
ergy crops. There are a large number of po-
tential candidates about which relatively little
is known (24). We need to understand where
these species can be grown, their environmen-
tal and ecological effects, their response to envi-
ronmental conditions, biotic and abiotic sensi-
tivities, genetic diversity, breeding systems, and
agronomic characteristics.
In light of environmental factors, and be-
cause water is limiting in most regions where
land may be available for production of cellu-
losic crops (28), perennial C4 grasses and sug-
arcane are likely to contribute a majority of
production. The diversity of C4 species may fa-
cilitate the selection of plants from nature to
meet particular environmental conditions, such
as salt tolerance, without the need for genetic
engineering. Woody species may be preferable
on certain soil types or on terrains that are too
irregular to allow machine harvesting of grasses.
In the near term, woody species may have ad-
vantages over grasses because of the existence of
large established stands and consolidated own-
ership that facilitates the practical aspects of ob-
taining enough biomass to support a processing
facility.
Although many species are promising candi-
dates as energy crops (24), several species have
received the most attention in Europe and the
Americas. Sugarcane is likely to be the most im-
portant energy crop for the foreseeable future
because it is well known, highly productive, and
can be used for both sugar and lignocellulose.
Although sugar comprises only approximately
14% of the cane dry weight, the high produc-
tivity of sugarcane (up to 100 t/ha) under low
input agriculture results in a high net energy
efficiency when sugarcane is used to produce
ethanol (34). More than a billion tons of sugar-
cane is produced worldwide and approximately
40% of transportation fuel in Brazil is produced
from approximately 3.5 Mha of sugarcane (33).
At present, the bagasse that remains after the
sugar is recovered is used to produce heat and
power for the processing of sugar to ethanol
and in efficient mills in Brazil; the bagasse is
also used to produce electricity that is sold into
the grid (68). When technology for conversion
of lignocellulose to fuels is mature, sugars will
likely be produced from the bagasse to further
increase the yield of fuel (19). This production
would necessarily be accompanied by improve-
ments in energy efficiency of the sugar process-
ing so that not all the mass of the bagasse is
required for process heat and power and the
export of electricity to the grid, as is currently
the case (68).
One of the most intensively investigated po-
tential new bioenergy crops is Miscanthus, a C4
perennial grass native to Southeast Asia (52).
Most research and commercial production has
used a single sterile hybrid, Miscanthus × gi-
ganteus, that is thought to be a spontaneous hy-
brid between M. sinensis and M. sacchariflorus.
M. gigantaeus grows to a height of approxi-
mately 3.5 m and generates a deep root struc-
ture stretching down approximately 1.8 m.
M. gigantaeus stores nutrients in rhizomes,
into which it withdraws its aboveground nu-
trients prior to winter. Miscanthus has been
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successfully grown from the Mediterranean cli-
mate of Spain as far north as Scandanavia. A
meta-analysis of Miscanthus studies found an
average yield of 24.9 t/ha for a two- to three-
year-old field harvested before September (66).
A study in Illinois reported a three-year av-
erage of 30 t/ha (39). In side-by-side trials in
Illinois, switchgrass yielded only 10 t/ha. Typi-
cal harvesting practice is to wait until the crop
dries in the field over winter before harvest-
ing. This causes the loss of between 30% and
50% of harvestable biomass as the plant loses
leaves (58) and may not be the optimal prac-
tice for biofuels. Further research is required
to determine the best practices for harvesting
and storage. It may also be possible to iden-
tify useful genetic variation for improved stand
stability.
M. gigantaeus is propagated by planting
fragments of rhizomes, a relatively expen-
sive method (17). However, the seeded variety
M. sinensis is more productive than M. gigan-
taeus in some regions of Europe where side-by-
side trials have been performed (16). There is
still a great deal of uncertainty about the pro-
ductive life of a Miscanthus field under varying
conditions. A definitive answer to the question
is important, because the cost of establishment
is one of the largest costs associated with Mis-
canthus cultivation. In colder climates there
can be substantial loss of M. giganteus plants
over the first winter. A frost-resistant strain of
M. sinensis was bred specifically for this problem
(27).
As in the case of sugarcane (5, 21), Miscant-
hus does not have substantial requirements for
N fertilizer under some conditions. A meta-
analysis of Miscanthus studies found only a
weak correlation between N fertilizer and yield.
A recent 14-year trial at varying levels of ap-
plied N found no effect of nitrogen fertilizer on
yield (15). Another model indicated that Mis-
canthus could be grown with yields as high as 50
t/ha with sufficient irrigation, and water was the
main limiting factor on growth (17). Nitrogen-
fixing bacteria have been isolated from the roots
of M. gigantaeus (23). The variance in reported
responses to nitrogen fertilizer is possibly due
174 Carroll · Somerville
to variations in the association with nitrogen-
fixing bacteria in the test fields. Further re-
search into the extent of nitrogen fixation of
field populations of Miscanthus is essential. If
the extent of nitrogen fixation is low, it may be
possible to improve Miscanthus yields on low
inputs through selective breeding or through
inoculating with organisms. If the extent of ni-
trogen fixation is as high as some studies indi-
cate, it should stimulate additional investigation
to understand the mechanisms involved. Per-
haps an opportunity exists to engineer nitrogen
fixation into grasses such as wheat, maize, and
rice.
Among fertile varieties of Miscanthus, most
species are self-incompatible, which has ren-
dered genetic studies challenging. However,
Chiang and coworkers (13) showed that an ac-
cession of M. sinensis var. Condensatus in Tai-
wan was self-compatible, possibly because of
strong selection from a high-salinity habitat
that limits diversity. A low-density marker map
for the Miscanthus genome has been gener-
ated from M. sinensis (2) and some quantitative
trait loci (QTL) analysis for selected agronomic
traits has been performed using this map (3).
Some lines of Miscanthus are allelopathic via
the production of phytotoxins (14). The extent
of allelopathy through the Miscanthus genus
is not well known, nor is it known how long
the phytotoxins would last or what species are
affected. Allelopathy could be considered de-
sirable in that it may reduce the need for
herbicides. Conversely, allelopathy might also
prevent mixed cropping, damage yields of
subsequently grown food crops, and inhibit
the growth of Miscanthus itself. Additional
research on the extent of allelopathy in Mis-
canthus and other energy crops may be useful.
Similar issues were associated with the devel-
opment of crops such as canola.
Switchgrass is a C4 perennial grass native
to the North American great plains that has
been the focus of most U.S. attention on bio-
fuel crops. Many different strains of switch-
grass are presently being grown in the United
States for forage, biomass, and to restore land
retired from agriculture. A meta-analysis of
 ANRV375-PP60-08 ARI 25 March 2009 13:17
switchgrass studies found an average yield of
12.1 t/ha (25). Switchgrass loses very little
biomass when harvested late in the fall, though
the nitrogen removed from switchgrass is sub-
stantially lower when harvest is delayed until
December. The U.S. Department of Energy
has supported efforts to develop switchgrass as
a biofuel crop, which has contributed greatly to
knowledge about switchgrass and to the devel-
opment of improved cultivars and agronomic
practices (80). Switchgrass yields increased by
∼50% from 1993 to 2003 (64).
Switchgrass has been suggested to be able to
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support a nitrogen-fixing association, although
the amount of nitrogen fixed is very low (3.9 kg
N/ha/y fixed as compared with 13 kg N/ha/y
provided by rainfall) (91). In a meta-analysis,
switchgrass had a much stronger response to N
fertilization than Miscanthus (41).
Switchgrass is variably polyploid. The two
dominant ecotypes differ in morphology, native
geography, and chromosome number. These
ecotypes have been designated lowland (L),
which is tetraploid, and upland (U), which is
either tetraploid or octaploid (48). Switchgrass
is self-incompatible, as are many other grasses
in the Poaceae family. Similar to many other
members of the family, the mechanism of in-
compatibility is the S-Z system, which involves
a pair of polyallelic genes that block pollen tube
germination if there is a compatible reaction.
A postfertilization system also prevents inter-
breeding between tetraploid and octaploid pop-
ulations (61). No allelopathy has been reported
in switchgrass.
Missaoui and colleagues (67) have produced
a low-density linkage map for switchgrass. This
first map should be a starting point for a more
comprehensive map and for the development of
QTL mapping for desirable traits. Casler and
coworkers (8) have reported substantial differ-
ences between the suitability of switchgrass eco-
types at different latitudes. A thorough analysis
of ecotype performance in different conditions
is required to take full advantage of the diversity
in switchgrass.
In cold, wet climates, the falctata subspecies
of alfalfa is a promising candidate. This peren-
nial fixes nitrogen and has been previously stud-
ied as a forage crop (81).
WOODY SPECIES
Hybrid poplar is considered a promising candi-
date for a woody energy crop. The availability
of a genome sequence and an existing research
community should facilitate development of
improved varieties. A forestry model for poplar
predicts yields of 12.4 t/ha on nonirrigated, un-
fertilized land and 22.5 t/ha on irrigated, fertil-
ized land (20). A study in Quebec found yields
of 17.3 t/ha for poplar and 16.9 t/ha for wil-
low, another promising candidate, without fer-
tilizer or irrigation (56). A study that compared
Miscanthus against poplar and willow across
Eastern Europe and Central Asia found yields
on land very suitable for poplar and willow av-
eraged between 14 and 18 t/ha. Though this
yield was less than Miscanthus yields (between
17 and 26 t/ha), certain regions were preferable
for poplar and willow. These regions also pro-
duced a higher maximum yield (38.1 t/ha) than
Miscanthus (28.1 t/ha) (29). Selective breeding
to improve the yield and decrease the nitrogen
requirements of these species may benefit tim-
ber and paper production as well. One open
question is how long such yields are sustainable
without substantial nitrogen inputs.
The nitrogen-fixing tropical tree Leucaena
leucocephala will produce approximately 35 t/ha
and responds well to coppice harvesting (24).
Woody species will likely have a niche either in
degraded soils in the tropics that would benefit
from Leucaena or in colder climates that are not
productive enough to support annual harvests.
AGRONOMIC ASPECTS
As noted above, perennial energy crops hold
a number of advantages over annuals for cellu-
losic biofuel production. Annuals require plant-
ing each year, which requires fuel and labor and
results in the loss of soil carbon, whereas peren-
nial crops require planting every 7 to 25 years
(55). Perennials accumulate reserves in their
rhizomes or stolons, which once established
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allows them to compete with weeds and quickly
make a canopy, thereby extending their grow-
ing season relative to annuals. Perennials also
invest in an extensive root structure, which al-
lows them to tap into deep sources of water and
nutrients, and transfers carbon from the atmo-
sphere into the soil.
In contrast to traditional crop production,
which largely involves monocultures, bioen-
ergy crops may likely be grown as mixed stands
of many genotypes of one species or many
species. Tilman and colleagues (90) found that
highly degraded marginal land planted with 16
different species of perennial grasses was ap-
proximately 3.4 times as productive as a peren-
nial grass monoculture. Some of the effect is
thought to be due to the presence of nitrogen-
fixing species. However, a large-scale field trial
of switchgrass on apparently similar acres but
with applied nitrogen reported much higher
levels of production from a switchgrass mono-
culture (84), so additional research is neces-
sary to evaluate the circumstances under which
species diversity stimulates biomass accumula-
tion. Positive effects of species diversity have
also been seen in forestry. For example, planting
eucalyptus with certain nitrogen-fixing trees in-
creases overall yield (30). It seems likely that
diverse stands could be useful in suppressing
effects of pests and pathogens. The compo-
sition of hemicellulose and cellulose is suf-
ficiently similar among species with similar
growth habits that bioconversion processes can
likely be made robust to substantial chemical
composition diversity (Table 1). Because all the
aboveground biomass is harvested, and because
the harvest date need not coincide with matu-
ration of grain or other concerns of food crop
agronomy, the presence of mixed stands should
not pose a harvesting problem.
Though mixed stands are promising, a num-
ber of challenges exist. The research required
to improve numerous crops in parallel is sub-
stantial and methods of seed production are not
well developed for most candidate species. Im-
proved crops would be evaluated in relation to
an ecosystem instead of individual productivity.
Allelopathy between species would also need
176 Carroll · Somerville
evaluation. Ideal mixes would depend on en-
vironmental conditions. The use of a portfo-
lio of crops will improve yields, lower inputs,
and hedge against dead ends in crop develop-
ment, but it will also require plant breeders,
molecular biologists, and ecologists to work
closely together. A framework is needed for
evaluating and selecting grass communities for
maximizing yield as an extension to the se-
lected ecosystems shown in Reference 89. Addi-
tional mixed-stand experiments need to be per-
formed to supplement the sparse knowledge in
the area, and a model of grassland productivity
based on environmental and species character-
istics should be developed and then refined as
mixed stands and monocultures are commer-
cially grown.
THE CHALLENGE OF
MARGINAL LANDS
As world population and affluence continue to
increase, agriculture will have to produce an in-
creasing amount of food per unit of land. The
displacement of food crops by biofuel crops
would place upward pressure on food prices.
The world has a great deal of marginal land
that is unfavorable for food cultivation and
is presently unused. In addition, poor agri-
cultural management has severely degraded a
large amount of land, much of it to the point
that it is abandoned by agriculture. Field and
colleagues (28) estimated abandoned lands at
approximately 450 Mha worldwide, with the
highest concentration of abandoned land in the
Eastern and Midwestern United States. Addi-
tionally, a great deal of degraded land remains
under cultivation. These lands face additional
degradation to the point of abandonment as a
result of their continued use in intense agricul-
ture. Estimates of moderately degraded lands
(those lands with significant decreases in pro-
ductivity) are up to 910 Mha worldwide (18).
The combined abandoned and degraded land
area of 1460 Mha is substantial when com-
pared with the 5700 Mha used for agriculture
and animal production worldwide (26). Ideally,
biofuel crops would combat desertification on
 ANRV375-PP60-08 ARI 25 March 2009 13:17
these lands, and rehabilitate degraded lands for
a return to intensive food crop agriculture.
A grand challenge for plant biologists is
to identify the most highly productive plant
species that can be grown on the various types
of marginal or abandoned land, optimize the
genetics and production practices, and evaluate
any environmental risks or benefits that may
accrue from encouraging the widespread use of
such species for energy production. Success in
meeting this challenge will require an interdis-
ciplinary approach that incorporates knowledge
from many other disciplines.
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HOW MUCH FUEL COULD
BE PRODUCED?
An influential analysis by a group of U.S.
government scientists of how much biomass
could be available for bioenergy production in
the United States estimated that as much as
1.3 billion dry tons could be available annu-
ally by approximately 2030 (72). If 90% of the
sugars derived from the biomass were utilized
by a biological process for ethanol production
(i.e., 90% conversion efficiency), that amount
of biomass would produce approximately 130
billion gallons of cellulosic ethanol, equivalent
on an energy basis to approximately 87 billion
gallons of gasoline. To put that in perspective,
in 2006 the United States used 138 billion gal-
lons of gasoline, 44% of world consumption.
Estimates of how much energy could be
produced from biomass worldwide are quite
variable (86). Approximately 13.4% of global
energy consumption is currently obtained from
biomass, mostly in the developing world. How-
ever, essentially none of this derives from ded-
icated energy crops. Sims and colleagues (86)
estimate that by 2025, up to 22 Ej/y (1.3 billion
t of biomass, assuming ∼17 Mj/kg of biomass)
of energy crops may be produced. That esti-
mate seems quite conservative by comparison
with the analysis indicating that that much may
be available in the United States alone (72). An-
other analysis concluded that world biofuel pro-
duction could reach 164 Ej, or approximately
35% of world primary energy use, in 2005 (68).
The large variation in estimates reflects the
many different assumptions about land use that
enter into such calculations. Unfortunately,
the large variation in estimates provides rela-
tively poor support for rational energy policy
formulation.
The theoretical maximum photosynthetic
efficiency for C4 plants is approximately 6%
(96), but the amount of energy actually accumu-
lated in plant biomass is much less. Heaton and
coworkers (40) report that the highest recorded
productions on an annualized basis were 3.8%
for the tropical C4 cereal Pennisetum typhoides
(80 t/ha) and 3.7% for the C4 grass Echinochloa
polystachya (99 t/ha). Many factors affect overall
efficiency (96). Altering the angle of leaves so
that sunlight penetrates the canopy has a sub-
stantial effect.
Heaton and colleagues (39) recently re-
ported three-year average annualized photo-
synthetic efficiency of approximately 1.4% for a
Miscanthus plot at the University of Illinois. In
view of the fact that the canopy was photosyn-
thetically active for only approximately 45% of
the year, the actual efficiency was substantially
higher than 1.4% but below the efficiencies cal-
culated for the tropical species noted above.
Thus, to get a rough sense of what might be
possible we note that 1% photosynthetic effi-
ciency on 1% of the land (149 Mha) would be
approximately 3.7 TW, or approximately 27%
of all human energy use in 2001 of approxi-
mately 13.5 TW (425 Ej) (59).
CONCLUDING REMARKS
Sustainable large-scale production of cellulosic
biofuels will require integration of knowledge
across many disciplines. In the short term, the
major research opportunities for plant biolo-
gists seem to be in identifying promising species
and understanding how to produce them, in
evaluating environmental and ecological as-
pects of lignocellulose production, and in in-
forming the design of better catalysts for hy-
drolysis of biomass. A fascinating opportunity
also exists to understand the details of how
sugarcane and Miscanthus apparently obtain
www.annualreviews.org • Cellulosic Biofuels 177
 ANRV375-PP60-08 ARI 25 March 2009 13:17

nitrogen from symbionts. Improved under-
standing should facilitate management of the
capability in energy grasses as well as open-
ing up the possibility of transferring the trait
to other grasses such as wheat. In the longer
term, many opportunities will exist to mod-
ify bioenergy crops with regard to agronomic
traits and quality traits related to the compo-
sition of biomass. Many aspects of agronomic
trait improvement will benefit from advanced
knowledge of food crops. By contrast, because
biomass composition has not been a signifi-
cant priority in the development of most food
crops, a great deal of basic information is lack-
ing in that area and should be a fertile topic for
research.

DISCLOSURE STATEMENT
Chris Somerville is a significant shareholder in Mendel Biotechnology, Inc. and LS9 Inc., two
by Stanford University - Main Campus - Green Library on 05/28/12. For personal use only.

companies with R and D activities that include biofuels. Additionally, he receives research funding
Annu. Rev. Plant Biol. 2009.60:165-182. Downloaded from www.annualreviews.org

from BP PLC, a company with business interests in a wide range of products, including biofuels.

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Annual Review of
Plant Biology

Contents Volume 60, 2009

My Journey From Horticulture to Plant Biology

Jan A.D. Zeevaart p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 1
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Roles of Proteolysis in Plant Self-Incompatibility

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Yijing Zhang, Zhonghua Zhao, and Yongbiao Xue p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p21

Epigenetic Regulation of Transposable Elements in Plants
Damon Lisch p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p43
14-3-3 and FHA Domains Mediate Phosphoprotein Interactions
David Chevalier, Erin R. Morris, and John C. Walker p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p67
Quantitative Genomics: Analyzing Intraspecific Variation Using
Global Gene Expression Polymorphisms or eQTLs
Dan Kliebenstein p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p93
DNA Transfer from Organelles to the Nucleus: The Idiosyncratic
Genetics of Endosymbiosis
Tatjana Kleine, Uwe G. Maier, and Dario Leister p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 115
The HSP90-SGT1 Chaperone Complex for NLR Immune Sensors
Ken Shirasu p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 139
Cellulosic Biofuels
Andrew Carroll and Chris Somerville p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 165
Jasmonate Passes Muster: A Receptor and Targets
for the Defense Hormone
John Browse p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 183
Phloem Transport: Cellular Pathways and Molecular Trafficking
Robert Turgeon and Shmuel Wolf p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 207
Selaginella and 400 Million Years of Separation
Jo Ann Banks p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 223
Sensing and Responding to Excess Light
Zhirong Li, Setsuko Wakao, Beat B. Fischer, and Krishna K. Niyogi p p p p p p p p p p p p p p p p p p p p 239
Aquilegia: A New Model for Plant Development, Ecology, and
Evolution
Elena M. Kramer p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 261

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Environmental Effects on Spatial and Temporal Patterns of Leaf

and Root Growth
Achim Walter, Wendy K. Silk, and Ulrich Schurr p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 279
Short-Read Sequencing Technologies for Transcriptional Analyses
Stacey A. Simon, Jixian Zhai, Raja Sekhar Nandety, Kevin P. McCormick,
Jia Zeng, Diego Mejia, and Blake C. Meyers p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 305
Biosynthesis of Plant Isoprenoids: Perspectives for Microbial
Engineering
James Kirby and Jay D. Keasling p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 335
The Circadian System in Higher Plants
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Stacey L. Harmer p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 357

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A Renaissance of Elicitors: Perception of Microbe-Associated

Molecular Patterns and Danger Signals by Pattern-Recognition
Receptors
Thomas Boller and Georg Felix p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 379
Signal Transduction in Responses to UV-B Radiation
Gareth I. Jenkins p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 407
Bias in Plant Gene Content Following Different Sorts of Duplication:
Tandem, Whole-Genome, Segmental, or by Transposition
Michael Freeling p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 433
Photorespiratory Metabolism: Genes, Mutants, Energetics,
and Redox Signaling
Christine H. Foyer, Arnold Bloom, Guillaume Queval, and Graham Noctor p p p p p p p p p p p 455
Roles of Plant Small RNAs in Biotic Stress Responses
Virginia Ruiz-Ferrer and Olivier Voinnet p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 485
Genetically Engineered Plants and Foods: A Scientist’s Analysis
of the Issues (Part II)
Peggy G. Lemaux p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 511
The Role of Hybridization in Plant Speciation
Pamela S. Soltis and Douglas E. Soltis p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 561
Indexes
Cumulative Index of Contributing Authors, Volumes 50–60 p p p p p p p p p p p p p p p p p p p p p p p p p p p 589
Cumulative Index of Chapter Titles, Volumes 50–60 p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 594
Errata
An online log of corrections to Annual Review of Plant Biology articles may be found at
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vi Contents