Special Focus Issue – Mini Review
Starch Accumulation in the Bundle Sheaths of C3 Plants: A
Possible Pre-Condition for C4 Photosynthesis
Hiroshi Miyake*
Graduate School of Bioagricultural Sciences, Nagoya University, Chikusa, Nagoya, 464-8601 Japan
*Corresponding author: E-mail, [email protected]; Fax, +81-52-789-4064.
(Received September 30, 2015; Accepted February 20, 2016)
C4 plants have evolved >60 times from their C3 ancestors. C4
photosynthesis requires a set of closely co-ordinated anatomical and biochemical characteristics. However, it is
now recognized that the evolution of C4 plants requires
fewer changes than had ever been considered, because of
the genetic, biochemical and anatomical pre-conditions of
C3 ancestors that were recruited into C4 photosynthesis.
Therefore, the pre-conditions in C3 plants are now being
actively investigated to clarify the evolutionary trajectory
from C3 to C4 plants and to engineer C4 traits efficiently
into C3 crops. In the present mini review, the anatomical
characteristics of C3 and C4 plants are briefly reviewed and
the importance of the bundle sheath for the evolution of C4
photosynthesis is described. For example, while the bundle
sheath of C3 rice plants accumulates large amounts of starch
in the developing leaf blade and at the lamina joint of the
mature leaf, the starch sheath function is also observed
during leaf development in starch accumulator grasses regardless of photosynthetic type. The starch sheath function
of C3 plants is therefore also implicated as a possible precondition for the evolution of C4 photosynthesis. The phylogenetic relationships between the types of storage carbohydrates and of photosynthesis need to be clarified in the
future.
Keywords: Bundle sheath C3 plant C4 plant Evolution Kranz sheath Starch sheath.
Abbreviations: PEPC, phosphoenolpyruvate carboxylase;
Rubisco, ribulose bisphosphate carboxylase/oxygenase.
Introduction
C4 photosynthesis consists of two types of spatially separated
carbon fixation steps (Edwards et al. 2004, Langdale 2011, Sage
et al. 2014). First, atmospheric CO2 is assimilated by phosphoenolpyruvate carboxylase (PEPC) in the form of bicarbonate to
produce C4 dicarboxylic acids. In the second step, CO2 is
released from the C4 dicarboxylic acids and fixed again by ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) to produce carbohydrates in the Calvin cycle. Spatial separation of
these two processes is essential to avoid competition in CO2
fixation between PEPC and Rubisco. If these mechanisms are
separated and the decarboxylation of C4 dicarboxylic acids is
sufficiently efficient, CO2 concentration around Rubisco
increases and the oxygenase activity of Rubisco is suppressed.
Thus, the photosynthetic efficiency is higher in C4 than C3
photosynthesis because energy wastage by photorespiration is
reduced. Although variations exist concerning the way in which
the two mechanisms are separated (Edwards and
Voznesenskaya 2011), most C4 plants utilize two distinct
chlorenchymatous tissues, namely mesophyll cells and bundle
sheath cells. The leaf structure of this type of C4 plant shows
Kranz anatomy, in which a layer of bundle sheath cells surrounds the vascular bundle and another layer of mesophyll
cells surrounds the bundle sheath, thus forming two concentric
layers of chlorenchymatous tissues around the vascular bundle
(Fig. 1B, C). Bundle sheath cells of C4 plants function as Kranz
cells, which conduct the second step of C4 photosynthesis
(Brown 1975, Sage et al. 2014). Mesophyll cells of C3 plants
are generally not arranged in a circular layer around the
bundle sheath; rather, up to 20 mesophyll cells are located
between the neighboring vascular bundles (Fig. 1A)
(Langdale 2011). It is noteworthy that C3 plants also possess
bundle sheaths (Esau 1977), and a critical difference between C3
and C4 plants is the number of mesophyll cells between bundle
sheaths (Crookston and Moss 1974).
C4 plants have independently evolved from C3 plants at least
66 times within the past 35 million years (Sage et al. 2012). All
enzymes required for C4 photosynthesis are already present in
C3 plants and were recruited into C4 photosynthesis during
evolution (Aubry et al. 2011, Brown et al. 2011, Williams et al.
2012, Külahoglu et al. 2014). However, fully operational C4
photosynthesis requires the establishment of proper structure–function relationships provided by a number of modifications to the genes, enzymes and gene expression (Hibberd and
Covshoff 2010, Sage et al. 2014). Similarly, in most C4 plant
lineages, bundle sheath cells are recruited for the localization
of the Calvin cycle. When we consider the evolutionary processes required to move from C3 to C4 photosynthesis and
attempt to engineer C4 photosynthesis into C3 crops, it is
important that we understand the relationship of the bundle
sheaths between C3 and C4 plants and the potential function of
the bundle sheath in C3 plants, which might be co-opted in C4
photosynthesis. In this mini review, starch accumulation in the
bundle sheaths of some C3 plants is described and its relevance
to C4 photosynthesis is discussed.
Plant Cell Physiol. 57(5): 890–896 (2016) doi:10.1093/pcp/pcw046, Advance Access publication on 2 March 2016,
available online at www.pcp.oxfordjournals.org
! The Author 2016. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists.
All rights reserved. For permissions, please email: [email protected]
Plant Cell Physiol. 57(5): 890–896 (2016) doi:10.1093/pcp/pcw046
Fig. 1 Light micrographs of transverse sections of grass leaves. (A) Fresh section of a flag leaf of rice, a C3 plant. (B) Zea mays, an NADP-malic
enzyme-type C4 plant. Note the centrifugal orientation of the bundle sheath chloroplasts. (C) Eleusine coracana, an NAD-malic enzyme-type C4
plant. Note the centripetal orientation of the bundle sheath chloroplasts. (D–F) Distribution of starch grains in rice leaves visualized by I–KI
(iodine in potassium iodide solution) staining. (D) Note a high accumulation of starch in the bundle sheath cells in the second leaf blade of a
seedling. (E) Bundle sheath cells accumulate a large amount of starch at the base of an emerging seventh leaf blade of rice grown in a paddy. (F)
Mature second leaf blade dissected, floated on distilled water and illuminated for 48 h. Note the high accumulation of starch in the bundle sheath
cells. Scale bars = 100 mm (A–E), 50 mm (F). BS, bundle sheath cell; LVB, large vascular bundle; M, mesophyll cell; MS, mestome sheath cell; SVB,
small vascular bundle.
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H. Miyake | Bundle sheath in C3 plants
The Bundle Sheath and the Kranz Sheath
Function
The bundle sheath is a layer or layers of cells enclosing a vascular
bundle in a leaf (Esau 1977). There is usually one layer of bundle
sheath cells in eudicots, but C3 grass species have two kinds of
bundle sheaths around large vascular bundles; an outer parenchyma sheath and an inner mestome sheath with thickened
walls. The parenchyma sheath has chloroplasts, while the mestome sheath typically possesses no chloroplasts (Brown 1975)
or undifferentiated proplastid-like structures (Esau 1977),
although the mestome sheaths of some C3 Neurachninae species (Hattersley et al. 1986) and a C3 subspecies of Alloteropsis
semialata (Ueno and Sentoku 2006) contain substantial numbers of chloroplasts. The mestome sheath is thought to be
homologous to the endodermis in roots and some stems
(Brown 1958, O’Brien and Carr 1970, Esau 1977); however,
it has recently been proposed that the parenchyma sheath is
homologous to the endodermis, and the mestome sheath is
derived from the pericycle (Martins and Scatene 2011,
Slewinski 2013).
The Kranz sheath, or the sheath of Kranz cells, of C4 grasses
can be derived from either of the two bundle sheaths of C3
ancestors, or both in the case of Aristida (Brown 1975).
However, the Kranz cells of Cyperaceae species, except those
having the Rhynchosporoid anatomy, are derived from the
pericycle inside the mestome sheath and are not homologous
to the bundle sheath cells (Martins and Scatena 2011).
Possible Functions of the Bundle Sheath in C3
Plants
The bundle sheath chloroplasts of rice, a C3 plant, are smaller
than mesophyll chloroplasts and their profiles are lens shaped,
while mesophyll chloroplasts are somewhat amorphous with
extended stromal regions (Fig. 2A, B) (Sage and Sage 2009,
Yamane et al. 2012). However, a comparable amount of
Rubisco is detected in the bundle sheath and mesophyll chloroplasts (Yamane et al. 2003), suggesting that the Calvin cycle is
operative in both chloroplasts. Functions other than photosynthesis of the bundle sheath in C3 plants have been suggested
based on anatomical characteristics. Among them are the provision of mechanical support and the transport and storage of
water and photoassimilates (Esau 1965, Kinsman and Pyke
1998). Recent advances in biochemistry and molecular biology
techniques have revealed roles for the bundle sheath in various
functions, including the synthesis and transport of carbohydrates, the assimilation and transport of nitrogen and sulfur,
and antioxidant metabolism (reviewed by Leegood 2008).
Roles in controlling hydraulic fluxes and cavitation repair have
also been proposed (Griffiths et al. 2013). Bundle sheath cells are
functionally different depending on their position around the
vascular bundle. The bundle sheath cells associated with the
phloem are involved in sugar transport, whereas those abutting
the xylem are involved in mineral transport (Cui et al. 2014).
Most of these functions seem to be incorporated into C4 plants,
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but others are reconstructed and recruited into C4 photosynthesis. For example, green cells around the vascular bundle in the
stems and leaf stalks of the C3 plants tobacco and celery have
the capacity to decarboxylate malate derived from the vascular
bundle and reassimilate CO2 into sugars using Rubisco (Hibberd
and Quick 2002). Three decarboxylating enzymes used in C4
photosynthesis are also detected in these cells. This mechanism
may play a role in conserving carbon derived from the root and
might be recruited into C4 photosynthesis.
In the following sections, the starch-accumulating activity of
the bundle sheaths in C3 plants will be discussed as a possible
pre-condition recruited into C4 photosynthesis.
The Bundle Sheath of Rice Functions as a
Starch Sheath
During the leaf development of rice, starch is accumulated in
the immature chloroplasts of both mesophyll and bundle
sheath cells, with much higher levels of starch accumulated in
the latter (Fig. 1D, E), which have amyloplast-like profiles
(Fig. 2C, D) (Miyake and Maeda 1976a). Starch grains are dissipated during leaf maturation, and the amyloplast-like structures in bundle sheath cells develop into mature chloroplasts.
The accumulation and dissipation of starch during leaf development also occurs in the dark; therefore, this starch is not
assimilatory but a storage type derived from carbohydrates in
other organs (transitory starch according to Sato 1984). This
starch is presumed to be used as a carbon and energy source
during leaf development. The bundle sheath chloroplasts of
Phragmites australis (formerly P. communis, C3) and Cynodon
dactylon (C4) also accumulate large amounts of storage starch
in the early stages of leaf development (Miyake and Maeda
1978). Grass species can be classified into three groups,
namely fructan (fructosan), starch and sucrose accumulators,
according to the major component of the storage carbohydrates in the vegetative tissues (Ojima and Isawa 1967,
Smouter and Simpson 1989). In addition, Smith (1968) classified grass species into two groups, fructan and starch accumulators, based on storage polysaccharides. Rice, P. australis and C.
dactylon are typical starch accumulators. Although limited
numbers of species were examined, it seems likely that
bundle sheath chloroplasts of starch accumulators, regardless
of photosynthetic type, are specialized in starch accumulation
during leaf development.
Types of major storage carbohydrates and their occurrence
in the clades of Poaceae are summarized in Table 1. Although
available data are limited, some relationships between carbohydrates and taxonomy have been detected. The types of storage carbohydrates are largely correlated with tribes, although
heterogeneous tribes exist in the PACMAD clade. Most tribes of
the Pooideae are fructan accumulators, except for Stipeae,
which consists of sucrose accumulators. At present, all of the
fructan accumulators are C3 plants (Bender and Smith 1973,
Muguerza et al. 2013), while C4 plants consist of starch accumulators and also sucrose accumulators to a lesser extent. It is
necessary to examine whether starch accumulators other than
Plant Cell Physiol. 57(5): 890–896 (2016) doi:10.1093/pcp/pcw046
Fig. 2 Electron micrographs of rice leaves. (A) Structure around a large vascular bundle of a fourth leaf blade. Note that the bundle sheath
chloroplasts are located in the cell periphery. (B) Structure around a small vascular bundle of a fourth leaf blade. Chloroplasts are seen in bundle
sheath cells. (C) Immature chloroplast with large starch grains showing an amyloplast-like profile in the bundle sheath cell of an emerging third
leaf blade. (D) Longitudinal view of a vascular bundle and adjacent bundle sheath cells and mesophyll cells of an emerging third leaf blade.
Note that the immature chloroplasts in bundle sheath cells accumulate large amounts of starch and show amyloplast-like profiles. Scale bars =
10 mm (A, B, D), 1 mm (C). BS, bundle sheath cell; Ch, chloroplast; M, mesophyll cell; MS, mestome sheath cell; S, starch grain; SE, sieve element; V,
vessel; VB, vascular bundle.
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H. Miyake | Bundle sheath in C3 plants
Table 1 Classification of grasses according to the major storage
carbohydrates in vegetative tissues
Taxona
Photosynthesisb Carbohydratec
PACMAD clade
Subfamily: Panicoideae
Paniceae (2)d
C4
Starch
Andropogoneae (4)
C4
Sucrose (3)/starch (1)
Paspaleae (1)
C4
Starch
Subfamily: Arundinoideae (1) C3
Subfamily: Danthonioideae (8) C3
Starch
Fructan (4)/sucrose (2)e
Subfamily: Chloridoideae
Eragrostideae (2)
C4
Starch
Zoysieae (4)
C4
Starch (3)/sucrose (1)
Cynodonteae (6)
C4
Starch
BEP clade
Subfamily: Ehrhartoideae
Oryzeae (1)
Ehrharteae (3)
C3
C3
Starch
Sucrose
C3
Sucrosef
Subfamily: Pooideae
Stipeae (7)
Bromeae (9)
C3
Fructan
Triticeae (6)
C3
Fructan
Poeae 2 (17)
C3
Fructan
Poeae 1 (13)
C3
Fructan
Classification is made at tribe level if available, otherwise at subfamily level.
a
Taxonomy follows GPWG II (2012).
b
Photosynthetic types of the species counted in the table. Tribes Paniceae and
Paspaleae contain both C3 and C4 plants (GPWG II 2012).
c
Classification with the major storage carbohydrates is compiled from the data
of Ojima and Isawa (1967), Smith (1968) and Smouter and Simpson (1989). The
data of dichotomy (fructan and starch accumulators) by Smith (1968) are
included if the content of fructan or starch is higher than that of non-reducing
free sugars to avoid confusion with sucrose accumulators.
d
Numbers in parentheses represent numbers of species reported.
e
Two species include both fructan and sucrose accumulators in different
habitats.
f
One species includes both sucrose and fructan accumulators in different
habitats.
those reported by Miyake and Maeda (1978) have a starch
sheath function. It is also important to accumulate data on
the type of storage carbohydrates in various taxa, which will
be discussed later.
After leaf maturation, assimilatory starch begins to accumulate in both the mesophyll and the bundle sheath chloroplasts
of rice. When leaf blades are detached and placed in distilled
water under illumination (Miyake and Maeda 1976b), bundle
sheath chloroplasts accumulate large amounts of starch
(Fig. 1F). Mature bundle sheath chloroplasts are smaller than
mesophyll chloroplasts but they are still active in starch
synthesis and storage, producing enough to occupy the entire
cell if translocation out of the leaf blade is blocked. It is of
interest that the bundle sheath cells of barley, a fructan
accumulator, show a tendency to accumulate more fructan
than mesophyll cells under high-light conditions (Koroleva et
al. 1998).
The expression of photosynthesis-related genes rbcS (a small
subunit of Rubisco) and cab (a light-harvesting Chl a/b protein)
was examined by in situ hybridization in emerging rice leaf
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blades (Tsutsumi et al. 2006, Tsutsumi et al. 2008). The expression of these genes was observed in both mesophyll and bundle
sheath cells in the basal (young) region of the leaf blades, but
was only observed in mesophyll cells in mature regions. This
suggests that bundle sheath chloroplasts are less active in
photosynthesis compared with mesophyll chloroplasts,
although Rubisco protein was retained in mature bundle
sheath chloroplasts (Yamane et al. 2003, Tsutsumi et al.
2008). From these observations, it is suggested that the
bundle sheath chloroplasts of rice leaf blades are more specialized in carbohydrate accumulation and that the bundle sheath
functions as a starch sheath (Esau 1977, Geldner 2013).
Starch Grains in the Bundle Sheath at the
Lamina Joint of Rice Function as a Statolith
The lamina joint is the junction between a leaf blade and a leaf
sheath. The lamina joint of rice bends in response to gravity
(Maeda 1960a), with an elongation of cells on the adaxial side
which induces inclination of the leaf blade in relation to the leaf
sheath (Maeda 1961). This geonastic response functions to
improve the light-intercepting characteristics of the rice
plant, as the lamina joint bends to make the leaf blade upright
if the plant body is lodged. Auxins (Maeda 1960b) and brassinosteroids (Takeno and Pharis 1982) are major phytohormones
concerned with the bending of lamina joints.
A large amount of starch is accumulated in the bundle
sheath cells and bundle sheath extension cells (parenchyma
cells extending from the bundle sheath towards the epidermis)
at the lamina joint of mature rice leaves. These starch grains are
proposed to function as statoliths, which sediment at the
bottom of the cell to enable the geonastic response of the
lamina joint (Nakano and Maeda 1978). If rice seedlings are
kept in the dark, starch grains in the bundle sheath cells in an
emerging leaf blade disappear during leaf maturation; however,
those of the lamina joint persist throughout development
(Tsutsumi et al. 2007). In a liguleless mutant, which has no
functional lamina joint, starch grains in the bundle sheath
cells at the blade–sheath boundary region, which corresponds
to the lamina joint of the wild type, disappear during leaf
maturation along with those in the leaf blade (Tsutsumi et al.
2007). It is therefore suggested that starch grains in the bundle
sheath cells of a leaf blade are accumulated and utilized for leaf
development, while those in the lamina joint function as a
statolith.
The endodermis in the stem of eudicots often accumulates
starch and is referred to as a starch sheath. The starch sheath
has the role of a carbohydrate reservoir, and the stored starch
may be preserved perennially in some plants (Van Fleet 1961).
In addition, starch grains in the endodermis function as a statolith and are essential for negative gravitropism of the shoot
(Fukaki et al. 1998, Kim et al. 2011). The physiology of the
eudicot endodermis is very similar to the bundle sheath of
rice, which is homologous to the endodermis (Slewinski
2013). It is of interest that the endodermis plays a role in
polar auxin transport (Slewinski et al. 2012).
Plant Cell Physiol. 57(5): 890–896 (2016) doi:10.1093/pcp/pcw046
The Starch Sheath Function and C4
Photosynthesis
The Kranz sheath of C4 plants also functions as a starch sheath
with respect to assimilatory starch (Laetsch 1974, Slewinski
2013). Bundle sheath chloroplasts of C4 plants accumulate
large amounts of starch during photosynthesis. This phenomenon occurs not only because the Calvin cycle is localized in
bundle sheath chloroplasts, but also because major enzymes in
starch synthesis preferentially accumulate in bundle sheath
chloroplasts (Weise et al. 2011). The starch sheath function of
the Kranz sheath is beneficial to C4 plants; starch synthesis and
accumulation in bundle sheath chloroplasts act as an overflow
mechanism for photosynthate and contribute to inorganic
phosphate recycling, allowing the Calvin cycle to proceed efficiently when the export of photosynthate and sucrose synthesis
are limited (Paul and Foyer 2001, Weise et al. 2011). In addition,
starch accumulation does not disturb the osmotic environment
within a cell to the same degree as sucrose accumulation. If the
bundle sheath chloroplasts of C3 ancestors had a capacity for
starch synthesis and accumulation, it might not be a high risk
for these plants to concentrate the Calvin cycle in bundle
sheath chloroplasts during the evolution of C4 photosynthesis.
It is often proposed that anatomical and biochemical preconditions exist in C3 ancestors and that they were recruited
into C4 photosynthesis during evolution (Slewinski 2013,
Lundgren et al. 2014). The starch sheath function to accumulate storage starch in C3 plants could be recruited into C4
photosynthesis to accumulate assimilatory starch into the
Kranz sheath.
Concluding Remarks and Future Research
In recent years, pre-conditions of C4 photosynthesis in C3 plants
and C3–C4 intermediate plants have drawn the attention of
researchers in the context of the evolutionary trajectory to C4
photosynthesis. C2 photosynthesis, where a photorespiratory
glycine shuttle operates to concentrate CO2 in proto-Kranz
cells, is well known as the bridge from C3 to C4 photosynthesis
(Sage et al. 2014). The Kranz cell-like function of the green cells
near the vascular bundles in stems and petioles of some C3
species (Hibberd and Quick 2002) is also an attractive pre-condition for potential adaptation to C4 photosynthesis. In the
present mini review, the starch sheath function of C3 plants,
especially rice, was described as another possible pre-condition
for C4 photosynthesis. However, the starch sheath function of C3
plants is not well known in the literature. This is probably
because the starch sheath function is only observable temporarily in developing leaf blades of starch accumulator grasses and in
the gravity-responsive regions of herbaceous species.
Further studies are needed to examine starch sheath function in different plant taxa. The results need to be phylogenetically correlated with the appearance of C4 plants to examine
the significance of the starch sheath as an evolutionary precondition. Phylogenetic relationships between the types of storage carbohydrates and photosynthesis also need to be clarified.
C4 plants are largely starch accumulators, but some are sucrose
accumulators. Lineages of C4 sucrose accumulators and their C3
ancestors are of particular interest, since starch sheath function
was not detected in sucrose accumulators (Miyake and Maeda
1978). These studies will provide further insight into the evolutionary processes from C3 to C4 photosynthesis and the engineering of C4 crops.
Disclosures
The authors have no conflicts of interest to declare.
References
Aubry, S., Brown, N.J. and Hibberd, J.M. (2011) The role of proteins in C3
plants prior to their recruitment into the C4 pathway. J. Exp. Bot. 62:
3049–3059.
Bender, M.M. and Smith, D. (1973) Classification of starch- and fructosanaccumulating grasses as C-3 or C-4 species by carbon isotope analysis. J.
Br. Grassl. Soc. 28: 97–100.
Brown, N.J., Newell, C.A., Stanley, S., Chen, J.E., Perrin, A.J., Kajala, K., et al.
(2011) Independent and parallel recruitment of preexisting mechanisms underlying C4 photosynthesis. Science 331: 1436–1439.
Brown, W.V. (1958) Leaf anatomy in grass systematics. Bot. Gaz. 119: 170–
178.
Brown, W.V. (1975) Variations in anatomy, associations, and origins of
Kranz tissue. Amer. J. Bot. 62: 395–402.
Crookston, R.K. and Moss, D.N. (1974) Interveinal distance for
carbohydrate transport in leaves of C3 and C4 grasses. Crop Sci. 14:
123–125.
Cui, H., Kong, D., Liu, X. and Hao, Y. (2014) SCARECROW, SCR-LIKE 23 and
SHORT-ROOT control bundle sheath cell fate and function in
Arabidopsis thaliana. Plant J. 78: 319–327.
Edwards, G.E. and Voznesenskaya E.V. (2011) C4 photosynthesis: Kranz
forms and single-cell C4 in terrestrial plants. In C4 photosynthesis and
Related CO2 Concentrating Mechanisms. Edited by Raghavendra, S.and
Sage, R.F. pp. 29–61. Springer Verlag, Heidelberg/Berlin.
Edwards, G.E., Franceschi, V.R. and Voznesenskaya, E.V. (2004) Single-cell
C4 photosynthesis versus the dual-cell (Kranz) paradigm. Annu. Rev.
Plant Biol. 55: 173–196.
Esau, K. (1965) Plant Anatomy, 2nd edn. John Wiley & Sons, New York.
Esau, K. (1977) Anatomy of Seed Plants, 2nd edn. John Wiley & Sons, New
York.
Fukaki, H., Wysocka-Diller, J., Kato, T., Fujisawa, H., Benfey, P.N. and Tasaka,
M. (1998) Genetic evidence that the endodermis is essential for shoot
gravitropism in Arabidopsis thaliana. Plant J. 14: 425–430.
Geldner, N. (2013) The endodermis. Annu. Rev. Plant Biol. 64: 531–558.
GPWG II (Grass Phylogeny Working Group II) (2012) New grass phylogeny
resolves deep evolutionary relationships and discovers C4 origins. New
Phytol. 193: 304–312.
Griffiths, H., Weller, G., Toy, L.F.M. and Dennis, R.J. (2013) You’re so vein:
bundle sheath physiology, phylogeny and evolution in C3 and C4
plants. Plant Cell Environ. 36: 249–261.
Hattersley, P.W., Wong, S.-C., Perry, S. and Roksandic, Z. (1986)
Comparative ultrastructure and gas exchange characteristics of the
C3–C4 intermediate Neurachne minor S.T. Blake (Poaceae). Plant Cell
Environ. 9: 217–233.
Hibberd, J.M. and Covshoff, S. (2010) The regulation of gene
expression required for C4 photosynthesis. Annu. Rev. Plant Biol. 61:
181–207.
Hibberd, J.M. and Quick, W.P. (2002) Characteristics of C4 photosynthesis
in stems and petioles of C3 flowering plants. Nature 415: 451–454.
895
H. Miyake | Bundle sheath in C3 plants
Kim, K., Shin, J., Lee, S.H., Kweon, H.S., Maloof, J.N. and Choi, G. (2011)
Phytochromes inhibit hypocotyl negative gravitropism by regulating
the development of endodermal amyloplasts through phytochromeinteracting factors. Proc. Natl. Acad. Sci. USA 108: 1729–1734.
Kinsman, E.A. and Pyke, K.A. (1998) Bundle sheath cells and cell-specific
plastid development in Arabidopsis leaves. Development 125: 1815–
1822.
Koroleva, O.A., Farrar, J.F., Tomos, A.D. and Pollock, C.J. (1998)
Carbohydrates in individual cells of epidermis, mesophyll, and bundle
sheath in barley leaves with changed export or photosynthetic rate.
Plant Physiol. 118: 1525–15325.
Külahoglu, C., Denton, A.K., Sommer, M., Mass, J., Schliesky, S., Wrobel, T.J.,
et al. (2014) Comparative transcriptome atlases reveal altered gene
expression modules between two Cleomaceae C3 and C4 plant species.
Plant Cell 26: 3243–3260.
Laetsch, W.M. (1974) The C4 syndrome: a structural analysis. Annu. Rev.
Plant Physiol. 25: 27–52.
Langdale, J.A. (2011) C4 cycles: past, present, and future research on C4
photosynthesis. Plant Cell 23: 3879–3892.
Leegood, R.C. (2008) Roles of the bundle sheath cells in leaves of C3 plants.
J. Exp. Bot. 59: 1663–1673.
Lundgren, M.R., Osborne, C.P. and Christin, P.A. (2014) Deconstructing
Kranz anatomy to understand C4 evolution. J. Exp. Bot. 65: 3357–3369.
Maeda, E. (1960a) Geotropic reaction of excised rice leaves. Physiol. Plant.
13: 204–213.
Maeda, E. (1960b) Interaction of gibberellin and auxins in lamina joints of
excised rice leaves. Physiol. Plant. 13: 214–226.
Maeda, E. (1961) Studies on the mechanism of leaf formation in crop
plants. II. Anatomy of the lamina joint in rice plant. Proc. Crop. Sci.
Soc. Jpn. 29: 234–239.
Martins, S. and Scatena, V.L. (2011) Bundle sheath ontogeny in Kranz and
non-Kranz species of Cyperaceae (Poales). Aust. J. Bot. 59: 554–562.
Miyake, H. and Maeda, E. (1976a) Development of bundle sheath chloroplasts in rice seedlings. Can. J. Bot. 54: 556–565.
Miyake, H. and Maeda, E. (1976b) The fine structure of plastids in various
tissues in the leaf blade of rice. Ann. Bot. 70: 1131–1138.
Miyake, H. and Maeda, E. (1978) Starch accumulation in bundle sheath
chloroplasts during the leaf development of C3 and C4 plants of the
Gramineae. Can. J. Bot. 56: 880–882.
Muguerza, M., Gondo, T., Yoshida, M., Kawakami, A., Terami, F., Yamada,
T., et al. (2013) Modification of the total soluble sugar content of the C4
grass Paspalum notatum expressing the wheat-derived sucrose:sucrose
1-fructosyltransferase and sucrose:fructan 6-fructosyltransferase genes.
Grassl. Sci. 59: 196–204.
Nakano, H. and Maeda, E. (1978) On starch statolith in the lamina joint of
rice plants. Proc. Crop Sci. Soc. Jpn. 47: 262–266.
O’Brien, T.P. and Carr, D.J. (1970) A suberized layer in the cell walls of the
bundle sheath of grasses. Aust. J. Biol. Sci. 23: 275–287.
Ojima, K. and Isawa, T. (1967) Physiological studies on carbohydrates of
forage plants. 2. Characteristics of carbohydrate compositions according to species of plants. J. Jpn. Grassl. Soc. 13: 39–50.
Paul, M.J. and Foyer, C.H. (2001) Sink regulation of photosynthesis. J. Exp.
Biol. 52: 1383–1400.
896
Sage, T.L. and Sage, R.F. (2009) The functional anatomy of rice leaves:
implications for refixation of photorespiratory CO2 and efforts to engineer C4 photosynthesis into rice. Plant Cell Physiol. 50: 756–772.
Sage, R.F., Khoshravesh, R. and Sage, T.L. (2014) From proto-Kranz to C4
Kranz: building the bridge to C4 photosynthesis. J. Exp. Bot. 65: 3341–
3356.
Sage, R.F., Sage, T.L. and Kocacinar, F. (2012) Photorespiration and the
evolution of C4 photosynthesis. Annu. Rev Plant Biol. 63: 19–47.
Sato, K. (1984) Starch granules in tissues of rice plants and their changes in
relation to plant growth. JARQ 18: 79–86.
Slewinski, T.L. (2013) Using evolution as a guide to engineer Kranz-type C4
photosynthesis. Front. Plant Sci. 4: 212.
Slewinski, T.L., Anderson, A.A., Zhang, C. and Turgeon, R. (2012) Scarecrow
plays a role in establishing Kranz anatomy in maize leaves. Plant Cell
Physiol. 53: 2030–2037.
Smith, D. (1968) Classification of several native North American grasses as
starch or fructosan accumulators in relation to taxonomy. J. Br. Grassl.
Soc. 23: 306–309.
Smouter, H. and Simpson, R.J. (1989) Occurrence of fructans in the
Gramineae (Poaceae). New Phytol. 111: 359–368.
Takeno, K. and Pharis, R.P. (1982) Brassinosteroid-induced bending of the
leaf lamina of dwarf rice seedlings: an auxin-mediated phenomenon.
Plant Cell Physiol. 23: 1275–1281.
Tsutsumi, K., Kawasaki, M., Taniguchi, M., Itani, T., Maekawa, M. and
Miyake, H. (2007) Structural and functional differentiation of bundle
sheath and mesophyll cells in the lamina joint of rice compared with
that in the corresponding region of the liguleless genotype. Plant Prod.
Sci. 10: 346–356.
Tsutsumi, K., Kawasaki, M., Taniguchi, M. and Miyake, H. (2008) Gene
expression and accumulation of Rubisco in bundle sheath and mesophyll cells during leaf development and senescence in rice, a C3 plant.
Plant Prod. Sci. 11: 336–343.
Tsutsumi, K., Taniguchi, Y., Kawasaki, M., Taniguchi, M. and Miyake, H.
(2006) Expression of photosynthesis-related genes during the leaf development of a C3 plant rice as visualized by in situ hybridization. Plant
Prod. Sci. 9: 232–241.
Ueno, O. and Sentoku, N. (2006) Comparison of leaf structure and photosynthetic characteristics of C3 and C4 Alloteropsis semialata subspecies.
Plant Cell Environ. 29: 257–268.
Van Fleet, D.S. (1961) Histochemistry and function of the endodermis. Bot.
Rev. 27: 165–220.
Weise, S.E., van Wijk, K.J. and Sharkey, T.D. (2011) The role of transitory
starch in C3, CAM, and C4 metabolism and opportunities for engineering leaf starch accumulation. J. Exp. Bot. 62: 3109–3118.
Williams, B.P., Aubry, S. and Hibberd, J.M. (2012) Molecular evolution of
genes recruited into C4 photosynthesis. Trends Plant Sci. 17: 213–220.
Yamane, K., Hayakawa, K., Kawasaki, M., Taniguchi, M. and Miyake, H.
(2003) Bundle sheath chloroplasts of rice are more sensitive to drought
stress than mesophyll chloroplasts. J. Plant Physiol. 160: 1319–1327.
Yamane, K., Mitsuya, S., Taniguchi, M. and Miyake, H. (2012) Salt-induced
chloroplast protrusion is the process of exclusion of ribulose-1,5bisphosphate carboxylase/oxygenase from chloroplasts into cytoplasm
in leaves of rice. Plant Cell Environ. 35: 1663–1671.