- Research article
- Open Access
Transcriptome sequencing and profiling of expressed genes in cambial zone and differentiating xylem of Japanese cedar (Cryptomeria japonica)
https://doi.org/10.1186/1471-2164-15-219
© Mishima et al.; licensee BioMed Central Ltd. 2014
- Received: 1 October 2013
- Accepted: 7 March 2014
- Published: 20 March 2014
The Erratum to this article has been published in BMC Genomics 2016 17:803
Abstract
Background
Forest trees have ecological and economic importance, and Japanese cedar has highly valued wood attributes. Thus, studies of molecular aspects of wood formation offer practical information that may be used for screening and forward genetics approaches to improving wood quality.
Results
After identifying expressed sequence tags in Japanese cedar tissue undergoing xylogenesis, we designed a custom cDNA microarray to compare expression of highly regulated genes throughout a growing season. This led to identification of candidate genes involved both in wood formation and later cessation of growth and dormancy. Based on homology to orthologous protein groups, the genes were assigned to functional classes. A high proportion of sequences fell into functional classes related to posttranscriptional modification and signal transduction, while transcription factors and genes involved in the metabolism of sugars, cell-wall synthesis and lignification, and cold hardiness were among other classes of genes identified as having a potential role in xylem formation and seasonal wood formation.
Conclusions
We obtained 55,051 unique sequences by next-generation sequencing of a cDNA library prepared from cambial meristem and derivative cells. Previous studies on conifers have identified unique sequences expressed in developing xylem, but this is the first comprehensive study utilizing a collection of expressed sequence tags for expression studies related to xylem formation in Japanese cedar, which belongs to a different lineage than the Pinaceae. Our characterization of these sequences should allow comparative studies of genome evolution and functional genetics of wood species.
Keywords
- Cryptomeria japonica
- cDNA library
- Microarray
- Cambium
Background
Wood represents the main source for terrestrial biomass production and is a major renewable resource for the timber, paper, and bioenergy industries [1]. Genomics approaches have been applied to explore the molecular basis of growth and development in a few forest tree species with economic relevance. Transcript profiling in trees has also specifically focused on wood formation (xylogenesis) because of the ecological significance of forest trees and the economic importance of wood [2–4]. Wood formation begins from the cambium and generates wood as the end product of secondary vascular system development, which proceeds from cell division to expansion, secondary wall formation, lignification, and finally programmed cell death [5, 6]. Notably, identification of accumulated expressed sequence tags (ESTs) and their expression pattern during wood formation has been achieved in target species for breeding, such as Pinus, Populus and Picea[1, 2, 6–14].
Japanese cedar (Cryptomeria japonica) is an allogamous coniferous species that relies on wind-mediated pollen and seed dispersal, and it is one of the most important forestry tree species in Japan. The Japanese cedar tree has excellent attributes (straight bole, rapid growth, ease of processing, and pleasant color and scent), and it has been used for house construction, to build wooden ships, barrels, and musical instruments, and for many products intended for daily use for hundreds of years [15]. More than 3,700 Japanese cedar trees have been planted throughout Japan, covering an area of 4.5 million ha and accounting for 44% of Japan’s artificial forests. Seventeen million seedlings are supplied as planting material for forestation every year, making this species very important for Japanese forestry today, as it has been since ancient times [16].
Next-generation sequencing can be a more efficient approach for obtaining functional genomic information. This type of sequencing can result in high transcriptome coverage depth and facilitates the de novo assembly of transcriptomes from species where full genomes do not exist [17, 18]. In addition, by simultaneously measuring the abundance of transcripts for thousands of genes with accumulated sequence information, microarray analysis promises a comprehensive understanding of regulatory gene functions and the growth and development of plants [19]. To understand the molecular mechanisms involved in wood formation and key targets for genetic manipulation and selection of superior wood quality, these techniques will be powerful and efficient tools [20]. The only molecular studies of wood formation in Japanese cedar have identified large numbers of genes that are expressed in male strobili [21]. However, very limited genomics and functional genomics resources related to wood formation are publicly available for Japanese cedar.
The first objective of this paper was to produce an extensive collection of sequenced ESTs found in xylem and cDNA clones to support manufacture of cDNA microarrays and gene discovery efforts in Japanese cedar. The next goal was to elucidate a comprehensive expression profile in the growing season using these microarrays. For this purpose, we identified 55,051 unique sequences by next-generation Roche 454 sequencing using a non-normalized cDNA library from the cambial meristem and its derivatives from Japanese cedar. To gain further insight into seasonal expression patterns, a custom cDNA microarray was designed from the cDNA library obtained and from EST data (inner bark data on ForestGen; http://forestgen.ffpri.affrc.go.jp) [22] and was used to investigate differential gene expression in Japanese cedar during wood formation.
Results and discussion
Microscopic observation of differentiating xylem
Cross-sections of cambial zone and differentiating xylem of Cryptomeria japonica trees. A. Cross-sections viewed under an ordinary light microscope (24 March) and pairs of ordinary (left) and polarizing (right) light microscope images for the same field (27 April, 22 June, 24 August and 7 October). B. Number of cells in cambial zone and differentiating xylem. Cells in differentiating xylem were categorized into expanding cells, thickening cells and lignifying cells in accordance with ordinary and polarizing light microscope observations.
The number of expanding tracheids in each radial file had significantly decreased from an average of 8.8 cells in samples taken on 22 June to an average of 1.7 cells in samples taken on 24 August (p < 0.01). This indicated that cell division activity in the cambial zone was lower than at earlier stages. Thus, the major activities in differentiating xylem that could be observed microscopically were secondary wall formation and lignification in the samples collected in August and October.
EST sequencing and de novo assembly
Summary of EST sequencing and de novo assembly. A) Size distribution and cumulative percentage of raw sequence reads. B) Size distribution and cumulative percentage of contigs. C) Size distribution and cumulative percentage of isotigs. D) Distribution of isotig sequence coverage.
C. japonica transcriptome sequencing and assembly summary
Sequence | Bases (Mbp) | |
---|---|---|
Sequencing | ||
Raw sequencing reads | 308,542 | 125.1 |
Average read length | 405.29 bp | |
Assembly | ||
Trashed | 9764 | |
Reads used in assembly | 298,778 | 121.2 |
Average read length | 405.69 bp | |
Contigs | ||
All contigs | ||
Reads assembled as contigs | 241,696 | 98.6 |
Number of contigs (over 100 bp) | 15,521 | 12.7 |
large contigs (over 500 bp) | ||
Number of contigs | 11,022 | 11.2 |
Average contigs size | 1,014 | |
Largest contigs length | 9,656 | |
N50 contig size | 1,102 | |
Isotigs | ||
Number of isotigs | 14,616 | 15.6 |
Average isotigs size | 1,069 | |
Largest isotigs length | 9,656 | |
N50 isotig size | 1,261 | |
Avrage contig count | 1.7 | |
Singletons | 40,435 | |
Unique sequences | 55,051 |
Sequence comparison with other species
Sequence similarities. A) Number of transcript sequences from C. japonica cambium region similar to sequences in the NCBI, TAIR, ForestGen, ForestGen_Xylem, pine, spruce, and poplar databases according to BLASTx and tBLASTx E-value cutoff values. B) Venn diagram showing the overlap between our collected unique sequences and sequences in four other databases according to a tBLASTx search (E-value <1e-5).
Therefore, our data are expected to be a useful resource for ESTs related to xylem or cambium development in Japanese cedar.
Identifying protein families represented in sequences by Pfam
Occurrence of the 20 most common Pfam domains in the predicted proteins of unique transcripts from cambium and differentiating xylem of C. japonica
Description of Pfam domain | Number of C. japonica transcriptsa | Pfam accession |
---|---|---|
Protein kinase domain | 563 | PF00069 |
NB-ARC domain | 486 | PF00931 |
Leucine-rich repeat | 197 | PF13855 (including PF07714) |
Tyrosine kinase | 174 | PF07714 |
RNA recognition motif | 173 | PF00076 |
Cytochrome P450 | 171 | PF00067 |
PPR repeat family | 129 | PF13041 |
UDP-glucoronosyl and UDP-glucosyl transferase | 113 | PF00201 |
Reverse transcriptase (RNA-dependent DNA polymerase) | 110 | PF00078 (including PF07727) |
WD domain, G-beta repeat | 102 | PF00400 |
TIR domain | 98 | PF01582 |
DEAD/DEAH box helicase | 91 | PF00270 |
Alpha/beta hydrolase fold | 82 | PF12697 |
AAA proteins | 80 | PF00004 |
RING finger domain | 78 | PF13639 |
ATP-binding domain of ABC transporters | 77 | PF00005 |
Sugar (and other) transporter | 72 | PF00083 |
SET domain | 67 | PF00856 |
Mitochondrial carrier protein | 65 | PF00153 |
Protein phosphatase 2C | 65 | PF00481 |
Identifying proteins according to clusters of orthologous groups (COGs) from seven eukaryotic genomes represented in sequences
Functional classification and relative levels of ESTs derived from cambium region of C. japonica. Values are shown as percentage of unique transcripts in the pool.
Identification of transcription factors
Identification of transcripts encoding putative transcription factors in cambium and differentiating xylem in C. japonica against Populus trichocarpa
TF family | Description | vs Populus | |
---|---|---|---|
ESTs | %* | ||
C3H | Zinc finger, C-x8-C-x5-C-x3-H type | 160 | 5.82 |
NAC | No apical meristem (NAM) domain | 157 | 5.71 |
PHD | Cys4--His--Cys3 zinc finger | 146 | 5.31 |
AP2-EREB | PAP2 domain | 139 | 5.06 |
HB | Homeobox domain | 126 | 4.58 |
bHLH | Helix-loop-helix DNA-binding domain | 123 | 4.47 |
SNF2 | ATP binding/DNA binding/helicase/nucleic acid binding | 116 | 4.22 |
WRKY | WRKY DNA-binding domain | 115 | 4.18 |
C2H2 | Zinc finger, C2H2 type | 113 | 4.11 |
MYB | Myb-like DNA-binding domain | 110 | 4.00 |
Orphans | antiporter/multidrug efflux pump/transporter | 107 | 3.89 |
MYB-related | N-terminal myb-domain | 95 | 3.46 |
ARF | Auxin response factor | 68 | 2.47 |
SET | SET domain | 61 | 2.22 |
bZIP | Basic leucine zipper (bZIP) motif | 59 | 2.15 |
Trihelix | Trihelix DNA-binding domain | 58 | 2.11 |
CCAAT | NUCLEAR FACTOR Y, SUBUNIT A10 | 54 | 1.96 |
G2-like | PRENYLATED RAB ACCEPTOR 1.G2 | 54 | 1.96 |
GRAS | GRAS protein | 54 | 1.96 |
TRAF | TRAF homology domain-containing protein | 48 | 1.75 |
ABI3VP1 | ABI3/VP1 protein | 44 | 1.60 |
MADS | DNA-binding and dimaerization domain | 41 | 1.49 |
FAR1 | N-terminal microtubule binding motor domain | 40 | 1.46 |
GNAT | GCN5-related N-acetyltransferase (GNAT) family protein | 39 | 1.42 |
mTERF | mitochondrial transcription termination factor family protein | 36 | 1.31 |
Jumonji | nucleic acid binding/zinc ion binding | 31 | 1.13 |
TCP | ATP binding/protein binding | 30 | 1.09 |
HSF | Heat shock factor | 26 | 0.95 |
C2C2-Dof | Dof zinc finger | 23 | 0.84 |
FHA | Forkhead domain | 23 | 0.84 |
DBP | protein phosphatase 2C | 22 | 0.80 |
CPP | copalyl pyrophosphate (CPP) of gibberellin biosynthesis | 21 | 0.76 |
zf-HD | zf-HD class homeobox domain | 21 | 0.76 |
LOB | LATERAL ORGAN BOUNDARIES | 20 | 0.73 |
SBP | SBP domain | 20 | 0.73 |
AUX/IAA | AUX/IAA family | 19 | 0.69 |
C2C2-GATA | GATA zinc finger | 19 | 0.69 |
ARID | AT-rich interaction domain | 17 | 0.62 |
HMG | HMG (high mobility group) domain | 17 | 0.62 |
PLATZ | Plant AT-rich sequnce and zinc-binding protein1 | 17 | 0.62 |
LUG | LEUNIG gene | 16 | 0.58 |
CAMTA | Calmodulin-binding transcription activators | 15 | 0.55 |
RWP-RK | RWP-RK domain-containing protein | 15 | 0.55 |
ARR-B | Arabidopsis response regulator B | 14 | 0.51 |
CSD | superoxide dismutase | 14 | 0.51 |
Tify | JASMONATE-ZIM-DOMAIN PROTEIN 6 | 14 | 0.51 |
BES1 | BRI1-EMS supressor | 13 | 0.47 |
E2F-DP | DNA binding/protein heterodimerization | 13 | 0.47 |
SWI/SNF-SWI | chromatin binding/protein binding | 10 | 0.36 |
Alfin-like | Cys4 zinc finger and His/Cys3 | 9 | 0.33 |
C2C2-YABBY | YABBY transcription activator | 9 | 0.33 |
GRF | Growth regulation factor1 | 9 | 0.33 |
BSD | BSD domain-containing protein | 8 | 0.29 |
EIL | Ethylene insensitivel (EIN3) | 8 | 0.29 |
OFP | predicted nuclear localization signal | 8 | 0.29 |
Pseudo ARR-B | Pseudo Arabidopsis response regulator B | 8 | 0.29 |
TUB | structural constituent of cytoskeleton | 8 | 0.29 |
C2C2-CO-like | CCT motif | 7 | 0.25 |
DDT | DDT domain-containing protein | 7 | 0.25 |
Sigma70-like | DNA binding/DNA-directed RNA polymerase | 7 | 0.25 |
SWI/SNF-BAF | SWIB complex BAF60b domain-containing protein | 7 | 0.25 |
GeBPD | NA-binding storekeeper protein-related | 6 | 0.22 |
LIM | LIM domain | 5 | 0.18 |
TAZ | TAZ zinc finger | 5 | 0.18 |
VOZ | VOZ domain | 5 | 0.18 |
Coactivator p15 | transcriptional coactivator p15 (PC4) family protein | 3 | 0.11 |
IWS1 | molecular_function unknown | 3 | 0.11 |
BBR/BPC | DNA binding | 2 | 0.07 |
PBF-2-like | peptidase/threonine-type endopeptidase | 2 | 0.07 |
Rcd1-like | RADICAL-INDUCED CELL DEATH1 | 2 | 0.07 |
SRS | Domain unknown function | 2 | 0.07 |
HRT | nucleotide binding | 1 | 0.04 |
MED6 | RNA polymerase transcriptional regulation mediator-related | 1 | 0.04 |
MED7 | MED7 domain | 1 | 0.04 |
RB | Retinoblastoma-associated protein B domain | 1 | 0.04 |
SOH1 | SOH1 domain | 1 | 0.04 |
ULT | DNA binding | 1 | 0.04 |
Identification of transcripts encoding putative transcription factors in cambium and differentiating xylem in C. japonica against Arabidopsis thaliana
TF family | Description | vs Arabidopsis | |
---|---|---|---|
ESTs | %* | ||
WRKY | WRKY DNA-binding domain | 218 | 7.07 |
MYB | Myb-like DNA-binding domain | 167 | 5.41 |
bHLH | Helix-loop-helix DNA-binding domain | 162 | 5.25 |
SNF2 | ATP binding/DNA binding/helicase/nucleic acid binding | 150 | 4.86 |
PHD | Cys4--His--Cys3 zinc finger | 148 | 4.80 |
Orphans | antiporter/multidrug efflux pump/transporter | 135 | 4.38 |
C3H | Zinc finger, C-x8-C-x5-C-x3-H type | 134 | 4.34 |
HB | Homeobox domain | 131 | 4.25 |
AP2-EREBP | AP2 domain | 130 | 4.21 |
C2H2 | Zinc finger, C2H2 type | 117 | 3.79 |
NAC | No apical meristem (NAM) domain | 104 | 3.37 |
MYB-related | N-terminal myb-domain | 83 | 2.69 |
SET | SET domain | 76 | 2.46 |
bZIP | Basic leucine zipper (bZIP) motif | 72 | 2.33 |
CCAAT | NUCLEAR FACTOR Y, SUBUNIT A10 | 61 | 1.98 |
ARF | Auxin response factor | 56 | 1.82 |
G2-like | PRENYLATED RAB ACCEPTOR 1.G2 | 51 | 1.65 |
HSF | Heat shock factor | 49 | 1.59 |
MADS | DNA-binding and dimaerization domain | 47 | 1.52 |
GRAS | GRAS protein | 45 | 1.46 |
C2C2-Dof | Dof zinc finger | 45 | 1.46 |
FHA | Forkhead domain | 45 | 1.46 |
ABI3VP1 | ABI3/VP1 protein | 43 | 1.39 |
Trihelix | Trihelix DNA-binding domain | 42 | 1.36 |
GNAT | GCN5-related N-acetyltransferase (GNAT) family protein | 39 | 1.26 |
Jumonji | nucleic acid binding/zinc ion binding | 39 | 1.26 |
mTERF | mitochondrial transcription termination factor family protein | 38 | 1.23 |
TRAF | TRAF homology domain-containing protein | 36 | 1.17 |
C2C2-GATA | GATA zinc finger | 32 | 1.04 |
LOB | LATERAL ORGAN BOUNDARIES | 31 | 1.00 |
AUX/IAA | AUX/IAA family | 25 | 0.81 |
DDT | DDT domain-containing protein | 25 | 0.81 |
FAR1 | N-terminal microtubule binding motor domain | 25 | 0.81 |
ARID | AT-rich interaction domain | 23 | 0.75 |
RWP-RK | RWP-RK domain-containing protein | 23 | 0.75 |
SBP | SBP domain | 23 | 0.75 |
CSD | superoxide dismutase | 21 | 0.68 |
ARR-B | Arabidopsis response regulator B | 20 | 0.65 |
DBP | protein phosphatase 2C | 19 | 0.62 |
TAZ | TAZ zinc finger | 18 | 0.58 |
zf-HD | zf-HD class homeobox domain | 18 | 0.58 |
BES1 | BRI1-EMS supressor | 16 | 0.52 |
E2F-DP | DNA binding/protein heterodimerization | 16 | 0.52 |
SWI/SNF-BAF60b | SWIB complex BAF60b domain-containing protein | 16 | 0.52 |
TUB | structural constituent of cytoskeleton | 16 | 0.52 |
C2C2-CO-like | CCT motif | 15 | 0.49 |
CPP | copalyl pyrophosphate (CPP) of gibberellin biosynthesis | 15 | 0.49 |
GRF | Growth regulation factor1 | 15 | 0.49 |
SWI/SNF-SWI3 | chromatin binding/protein binding | 14 | 0.45 |
GeBP | DNA-binding storekeeper protein-related | 13 | 0.42 |
Pseudo ARR-B | Pseudo Arabidopsis response regulator B | 13 | 0.42 |
TCP | ATP binding/protein binding | 13 | 0.42 |
Tify | JASMONATE-ZIM-DOMAIN PROTEIN 6 | 13 | 0.42 |
BSD | BSD domain-containing protein | 12 | 0.39 |
HMG | HMG (high mobility group) domain | 12 | 0.39 |
LUG | LEUNIG gene | 12 | 0.39 |
CAMTA | Calmodulin-binding transcription activators | 11 | 0.36 |
PLATZ | Plant AT-rich sequnce and zinc-binding protein1 | 11 | 0.36 |
Alfin-like | Cys4 zinc finger and His/Cys3 | 10 | 0.32 |
EIL | Ethylene insensitivel (EIN3) | 10 | 0.32 |
SRS | Domain unknown function | 9 | 0.29 |
IWS1 | molecular_function unknown | 7 | 0.23 |
OFP | predicted nuclear localization signal | 7 | 0.23 |
Sigma70-like | DNA binding/DNA-directed RNA polymerase | 6 | 0.19 |
BBR/BPC | DNA binding | 5 | 0.16 |
PBF-2-like | peptidase/threonine-type endopeptidase | 5 | 0.16 |
VOZ | VOZ domain | 4 | 0.13 |
LIM | LIM domain | 3 | 0.10 |
RB | Retinoblastoma-associated protein B domain | 3 | 0.10 |
Rcd1-like | RADICAL-INDUCED CELL DEATH1 | 3 | 0.10 |
SAP | STERILE APETALA domain | 3 | 0.10 |
Coactivator p15 | transcriptional coactivator p15 (PC4) family protein | 2 | 0.06 |
C2C2-YABBY | YABBY transcription activator | 2 | 0.06 |
S1Fa-like | DNA binding protein S1FA | 2 | 0.06 |
HRT | nucleotide binding | 1 | 0.03 |
LFY | Floricaula/Leafy protein | 1 | 0.03 |
MBF1 | Multiprotein bridging factor 1 | 1 | 0.03 |
MED6 | RNA polymerase transcriptional regulation mediator-related | 1 | 0.03 |
SOH1 | SOH1 domain | 1 | 0.03 |
Comprehensive gene expression changes during xylem formation
Co-regulation patterns of differentially accumulated transcripts in xylem formation. A total of 10,380 transcripts differentially accumulated in xylem formation were clustered into 14 groups using the Pearson correlation on the Subio platform. The graphs show the average expression profile of each cluster; changes are on a log2 scale. The gene expression pattern is shown as A) upregulation and B) downregulation during xylem formation. The description and expression profile of the individual targets are summarized in Additional file 2.
Number of differentially expressed genes according to their cluster and functional COG classification
A1 | A2 | A3 | A4 | A5 | A6 | A7 | B1 | B2 | B3 | B4 | B5 | B6 | B7 | ||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
[A] | RNA processing and modification | 3 | 0 | 6 | 3 | 11 | 21 | 0 | 3 | 23 | 9 | 4 | 15 | 60 | 123 |
[B] | Chromatin structure and dynamics | 1 | 0 | 7 | 0 | 13 | 2 | 4 | 8 | 10 | 1 | 1 | 5 | 18 | 78 |
[C] | Energy production and conversion | 20 | 0 | 25 | 26 | 37 | 29 | 0 | 8 | 31 | 18 | 0 | 6 | 32 | 10 |
[D] | Cell cycle control, cell division, chromosome partitioning | 1 | 0 | 8 | 4 | 23 | 5 | 0 | 3 | 12 | 3 | 0 | 2 | 20 | 21 |
[E] | Amino acid transport and metabolism | 7 | 2 | 32 | 11 | 39 | 28 | 4 | 10 | 23 | 16 | 1 | 7 | 8 | 53 |
[F] | Nucleotide transport and metabolism | 0 | 0 | 2 | 0 | 12 | 11 | 0 | 1 | 8 | 2 | 2 | 4 | 6 | 15 |
[G] | Carbohydrate transport and metabolism | 9 | 0 | 65 | 26 | 113 | 41 | 9 | 29 | 32 | 23 | 2 | 19 | 69 | 47 |
[H] | Coenzyme transport and metabolism | 11 | 0 | 2 | 7 | 19 | 7 | 1 | 1 | 8 | 2 | 0 | 1 | 3 | 5 |
[I] | Lipid transport and metabolism | 6 | 0 | 34 | 10 | 53 | 33 | 9 | 13 | 37 | 18 | 1 | 18 | 17 | 40 |
[J] | Translation, ribosomal structure and biogenesis | 7 | 0 | 28 | 1 | 11 | 8 | 0 | 35 | 9 | 5 | 0 | 4 | 13 | 42 |
[K] | Transcription | 15 | 2 | 19 | 7 | 30 | 23 | 3 | 12 | 59 | 24 | 2 | 20 | 91 | 98 |
[L] | Replication, recombination and repair | 0 | 0 | 8 | 5 | 8 | 4 | 2 | 7 | 16 | 4 | 1 | 5 | 18 | 35 |
[M] | Cell wall/membrane/envelope biogenesis | 2 | 1 | 29 | 9 | 65 | 17 | 5 | 11 | 19 | 3 | 0 | 3 | 14 | 38 |
[N] | Cell motility | 0 | 0 | 0 | 2 | 1 | 0 | 0 | 0 | 1 | 0 | 0 | 0 | 1 | 2 |
[O] | Posttranslational modification, protein turnover, chaperones | 18 | 0 | 30 | 37 | 51 | 84 | 29 | 21 | 44 | 33 | 10 | 20 | 62 | 110 |
[P] | Inorganic ion transport and metabolism | 9 | 0 | 24 | 8 | 11 | 15 | 5 | 7 | 8 | 8 | 1 | 9 | 12 | 48 |
[Q] | Secondary metabolites biosynthesis, transport and catabolism | 8 | 2 | 17 | 11 | 50 | 31 | 9 | 18 | 68 | 36 | 1 | 7 | 36 | 48 |
[R] | General function prediction only | 16 | 0 | 104 | 52 | 133 | 121 | 26 | 45 | 159 | 60 | 7 | 50 | 132 | 263 |
[S] | Function unknown | 18 | 0 | 61 | 23 | 87 | 39 | 5 | 22 | 37 | 50 | 4 | 33 | 68 | 69 |
[T] | Signal transduction mechanisms | 23 | 4 | 97 | 22 | 126 | 40 | 32 | 51 | 77 | 40 | 10 | 88 | 144 | 435 |
[U] | Intracellular trafficking, secretion, and vesicular transport | 5 | 0 | 48 | 26 | 45 | 17 | 3 | 20 | 12 | 6 | 0 | 8 | 25 | 28 |
[V] | Defense mechanisms | 2 | 0 | 8 | 8 | 35 | 19 | 7 | 19 | 20 | 15 | 3 | 55 | 64 | 227 |
[W] | Extracellular structures | 1 | 0 | 2 | 1 | 22 | 2 | 1 | 0 | 0 | 0 | 0 | 0 | 1 | 3 |
[X] | Unassigned | 21 | 2 | 70 | 25 | 123 | 67 | 24 | 19 | 87 | 36 | 5 | 43 | 98 | 146 |
[Y] | Nuclear structure | 1 | 0 | 3 | 0 | 1 | 0 | 1 | 5 | 1 | 0 | 0 | 3 | 0 | 9 |
[Z] | Cytoskeleton | 4 | 0 | 32 | 19 | 41 | 9 | 0 | 14 | 5 | 1 | 0 | 9 | 15 | 8 |
Cell-cycle related genes
Expression of cell-cycle genes in cambial region during xylem formation. The individual targets are summarized in Additional file 3. All expression data are presented on a log2 scale.
Xylogenesis genes related to phenylpropanoid metabolism
During the development of xylem tissue, primary cell wall biosynthesis, secondary wall deposition, and lignification are important fundamental processes, because of the need for maintaining biological mechanisms conferring adaptability to various environments, compressive strength and defense against pathogens. These processes are also important determinants of wood properties.
Expression of phenylpropanoid metabolism-related genes in cambial region during xylem formation. A) Upregulated genes involved in lignin biosynthesis. B) PAL4 (isotig 10873) and 4CL3 (isotig 11289). The individual targets are summarized in Additional file 3. All expression data are presented on a log2 scale.
Interestingly, enzymes in the early part of the monolignol pathway, acting between PAL and 4CL, are also involved in the biosynthesis of other phenylpropanoids, like flavonoids, coumarins, and stilbene [39]. Lignans, which are monolignol-derived dimers and oligomers involved in such processes as defense reactions, are synthesized through the same pathway [39]. The expression of PAL4 (isotig 10873) and 4CL3 (isotig 11289) was upregulated during dormancy and following cessation of growth (Figure 7B, Additional file 3), which indicates that these enzymes could play roles in defense, such as responses to infection, wounding, drought stress and temperature change.
Expression of peroxidase superfamily in cambial region during xylem formation. A) Genes upregulated in activity period. B) Genes upregulated during dormancy and cessation of growth. The individual targets are summarized in Additional file 3. All expression data are presented on a log2 scale.
Expression of laccase genes in cambial region during xylem formation. The individual targets are summarized in Additional file 3. All expression data are presented on a log2 scale.
Xylogenesis genes related to carbohydrate, cellulose, and hemicellulose metabolism
Expression of cellulose synthase and cellulose synthase-like genes in cambial region during xylem formation. The individual targets are summarized in Additional file 3. All expression data are presented on a log2 scale.
Expression of KORRIGAN1 and COBRA in cambial region during xylem formation. A) KORRIGAN1 (KOR1). B) COBRA (COB). The individual targets are summarized in Additional file 3. All expression data are presented on a log2 scale.
Expression of hemicellulose-related gene family in cambial region during xylem formation. The individual targets are summarized in Additional file 3. All expression data are presented on a log2 scale.
Expression of glycosyltransferase and xyloglucan endotransglycosylase in cambial region during xylem formation. A) Glycosyltransferase. B) Xyloglucan endotransglycosylase. The individual targets are summarized in Additional file 3. All expression data are presented on a log2 scale.
Expression of sucrose synthase, invertase, and sucrose phosphate synthase in cambial region during xylem formation. A) Sucrose synthase. B) Invertase. C) Sucrose phosphate synthase. The individual targets are summarized in Additional file 3. All expression data are presented on a log2 scale.
Transcription factors
Expression of cell wall-related transcription factors in cambial region during xylem formation. A) MYB. B) NAC. C) Other cell wall-related transcription factors (LIM, HB, b-ZIP, WRKY). The individual targets are summarized in Additional file 3. All expression data are presented on a log2 scale.
Hormonal regulation of the activity-dormancy cycle
Expression of hormonal regulation-related genes in cambial region during xylem formation. A) Auxin signaling and transport component. B) GA biosynthesis-related and signaling genes. C) ABA biosynthesis-related and signaling genes. The individual targets are summarized in Additional file 3. All expression data are presented on a log2 scale.
Gibberellins (GAs) act synergistically with auxin in stimulating cambial growth [95]. The analysis of transgenic aspen indicated that GAs are required both in xylogenesis, which is likely mediated by GA signaling in the cambium, and in fiber elongation in the developing xylem [96]. In angiosperm trees, application of GA results in the formation of wood fibers with enhanced thickness of the inner layers of cell walls [97, 98]. We found that a homolog of GA3-oxidase (GA3ox, Cj.17342_1), implicated in the last step of GA biosynthesis, and the receptor gene GID1 (Cj.5192_1, isotig13598) were moderately upregulated at peak xylem formation (Figure 16B, Additional file 3). The genes encoding GA biosynthetic enzymes GA20-oxidase (GA20ox) and GA3ox are particularly important for control of bioactive GA levels [99]. GA signaling operates as a derepressible system that is moderated by DELLA-domain proteins, which are transcriptional regulators that repress GA responses [99]. Like DELLA-domain proteins, the homologs of RGA (Cj 552_1, 1674_1) were expressed inversely to these genes (Figure 16B, Additional file 3). These findings suggest that genes involved in GA signaling have an important role in xylem formation.
Abscisic acid (ABA) content increases during abiotic stress, and especially protects plant water status. In poplar cambium, ABA levels are increased by short days and by short days with low temperature in late autumn and during cambial reactivation in early spring [36]. Genes related to ABA biosynthesis and signaling, such as ABA4, NCED, CYP707A, PP2C (HAI1, 2), SnRK2.6 (OST1), ABRE (ABI1, 5, ABF1), and PYL (1,4,10), were upregulated in March and October (Figure 16C, Additional file 3). Most of these genes were rapidly downregulated from March to April, suggesting that their downregulation is coincident with release from cold hardiness and the improvement in water deficit on cambial reactivation. The Arabidopsis CYP707A gene family (CYP707A1, 2), involved in ABA catabolism, controls seed dormancy [100]. Therefore, our observations suggest that ABA is degraded during cambial reactivation in Japanese cedar. In the apex of hybrid aspen, some 9-cis-epoxycarotenoid genes (such as NCED), which are involved in ABA biosynthesis, are induced after 5 weeks of short-day treatment, which also induces growth cessation [101]. As seen in our data (Figure 16C, Additional file 3), these genes (Cj13501_1, 2567_1, 8387_1) were upregulated in accordance with changes in day length. Other ABA biosynthesis-related and signaling genes were also upregulated from August to October, indicating they may be induced in response to several abiotic stresses (such as cold and drought) that also lead to cessation of growth (Figure 16C, Additional file 3).
Development of cold hardiness in activity-dormancy cycle
Expression of ICE1 in cambial region during xylem formation. The individual targets are summarized in Additional file 3. All expression data are presented on a log2 scale.
Expression of low temperature-induced genes in cambial region during xylem formation. Low temperature-induced and cold hardiness-related genes were clustered using the Pearson correlation on the Subio platform into three main patterns of expression during the autumn transition and early spring (clusters 1, 2) and during spring reactivation (cluster 3). The individual targets are summarized in Additional file 3. All expression data are presented on a log2 scale.
Expression of starch-breakdown related genes in cambial region during xylem formation. The individual targets are summarized in Additional file 3. All expression data are presented on a log2 scale.
Cytoskeleton-related genes
Expression of cytoskeleton related genes in cambial region during xylem formation. A) α/β-Tubulin. B) Actin, actin-related and actin interacting proteins. C) Kinesin gene family. D) Microtubule-associated protein gene family. The individual targets are summarized in Additional file 3. All expression data are presented on a log2 scale.
Actin forms microfilament structures by self-polymerization and interactions with numerous actin-binding proteins. In our data, the four homologs of atACT7 (isotigs 05994, 09744, 11932, and 14133) were upregulated during peak xylem formation, along with actin-related/interacting protein and a gene encoding a kinesin family protein (Figure 20B,C, Additional file 3). The homologs clustered closely in a group with a Pinus homolog in a phylogenetic tree of actin from Arabidopsis and the nearest sequences from other species [110]. atACT7 is preferentially expressed in younger, rapidly developing tissue, such as during germination and root growth in Arabidopsis[110, 111]. These findings correspond with our findings in developing xylem.
The organization and dynamics of microtubules are regulated by MAPs[108]. Our study found a gene encoding a MAP (MAP65-1: isotig 05735, 09873) that was more strongly transcribed than other MAP genes (Figure 20D, Additional file 3). AtMAP65-1 is able to promote tubulin polymerization, enhance microtubule nucleation, and decrease the critical concentration for tubulin polymerization [112]; this role agrees reasonably well with what would be expected from our expression pattern and anatomical observations.
Validation of microarray expression of 12 selected genes by qRT-PCR
Validation of microarray expression of 12 selected genes by qRT-PCR. A total of 12 genes were selected in the validation using qRT-PCR: (A) Phenylalanine ammonia-lyase (PAL: isotig 10873), (B) Cinnamate-4-hydroxylase (C4H: isotig 09462), (C) 4-Coumarate:CoA ligase (4CL: isotig 04988), (D) Hydroxycinnamoyl-CoA shikimate/quinate hydroxycinnamoyl transferase (HCT: isotig 10178), (E) p-Coumarate-3-hydroxylase (C3H: isotig 02271), (F) Caffeoyl-CoA O-methyltransferase; Cinnamyl alcohol dehydrogenase (CCoAOMT: isotig 10196), (G) Cinnamoyl-CoA reductase (CCR: isotig 05079), (H) Cinnamyl alcohol dehydrogenase (CAD: isotig 02638), (I) Sucrose synthase (Sus: isotig 12351), (J) Cellulose synthase (Ces: isotig 08498), (K) α-Tubulin (Tub α: isotig 02753), (L) β−Tubulin (Tub β: isotig 13384). In qRT-PCR, Ubiquitin (UBQ) was used as a reference gene, and the data were calibrated relative to transcript levels in the 24 March sample. Error bars show standard deviation for three replicates.
Conclusions
In this study, we obtained 55,051 unique sequences by sequencing a non-normalized cDNA library from the cambial meristem and derivative cells of Japanese cedar. A custom cDNA microarray was designed based on this library and EST data to investigate seasonal gene expression in Japanese cedar. This is the first comprehensive study of an extensive collection of EST sequences and expression studies related to xylem formation in Japanese cedar. Because Japanese cedar belongs to a different lineage than the Pinaceae, comparison of data could lead to significant findings on genome evolution in coniferous species. Our data may also be a useful resource for forward genetics and functional genetics studies in wood species.
Methods
Plant material
Tissue from the cambium region (including phloem and the differentiating xylem) was taken from four 15-year-old trees of Cryptomeria japonica plus-trees, clones Chousui8, Iiyama9, Nisihkawa10 and Tano1, in Hitachi, Ibaraki Prefecture for molecular analysis. The daily minimum and maximum temperatures were also recorded during the study (Additional file 4: Figure S2). The harvested tissues were immediately frozen in liquid nitrogen in the field, and then stored in the laboratory at −80°C for later RNA extraction. A square block (approximately 1 cm2) was collected for microscopy and fixed in FAA (formalin: acetic acid: 50% alcohol, 5:5:90) in the field. To evaluate how gene expression and morphological development in the cambial region changed over a single growing season, tissues from this region were collected from different trees at the same time (around 10 AM) on 15 different dates from 2010 to 2011: on 9 March, 9 April, 10 May, 1 June, 24 June, 16 July, 16 August, 19 September, 29 September, and 29 October in 2010 for construction of cDNA libraries and on 24 March, 27 April, 22 June, 22 August, and 7 October in 2011 for cDNA microarrays and for anatomical observation.
Anatomical observation of the cambial zone and the differentiating xylem
Small blocks were collected from stems corresponding to those used for microarray analysis. Thin sections were prepared from embedded tissue in blocks of LR White Resin (London Resin Co., Basingstoke, UK) and stained with safranin and Alcian blue 8GX. Anatomical observations were carried out under both an ordinary light microscope and a polarizing light microscope. The number of cells in the cambial zone and the number of expanding tracheids, secondary wall forming tracheids and lignified tracheids in each radial file were counted under the microscope. The number of cells at each growth stage was statistically compared by a Student’s t-test between samples.
RNA extraction and pyrosequencing
Total RNA was isolated from tissue of the cambium region and differentiating xylem of plus-trees using an RNeasy Plant Mini kit (Qiagen, Gaithersburg, MD, USA) for Chousui8 samples from ten different dates. The quality of total RNA was assessed by measuring the ratio of absorption at 260 nm and 280 nm via an Agilent Bioanalyzer 2100 (Agilent Technologies, Palo Alto, CA, USA). cDNA synthesis from a mixture of ten RNA samples, nebulization, adaptor ligation, emulsion PCR and sequencing were done at Hokkaido System Science Co., Ltd. (Sapporo, Hokkaido, Japan). Sequencing was performed using a Roche 454 Genome Sequencer platform (Roche/454 Life Sciences, Branford, CT, USA) with FLX or Titanium technology.
Assembly of ESTs from sequences obtained on the 454 platform
Using GS FLX pyrosequencing software, we selected high-quality sequences (> 99.0% accuracy on single base reads) for further processing and assembly. Trimmed and cleaned sequences were assembled using the cDNA assembly feature of Roche Newbler software v. 2.3 (Roche/454 Life Sciences). To obtain clean ESTs, adapter trimming and poly(A/T) removal were performed by the cutadapt tool [113], then short sequences (< 50 bp) were removed and the remaining sequences evaluated using the BLASTN algorithm against C. japonica microsatellite sequences obtained from NCBI (http://www.ncbi.nlm.nih.gov) [114], and Arabidopsis thaliana retrotransposon sequences obtained from TAIR (http://www.arabidopsis.org) [115]; reads with alignment length of 20 nt or more and percent identity of 90% or more were considered “hit reads” against these sequences. De novo assembly was performed using GS De Novo Assembler v2.3 (provided with the Roche GS FLX sequencer) with default parameters (minimum overlap length of 40, minimum percent identity of 90).
Functional annotation with the BLAST program
The assembled unique sequences putatively encoding proteins were searched against the Arabidopsis protein database in TAIR [115] and the NCBI non-redundant database [114] using the BLASTx algorithm. In addition, our transcripts were also searched against the ForestGEN database [22] using the tBLASTx algorithm. A typical cutoff E-value < 1e-5 was used. To identify known protein families, the unique sequences were also searched for the presence of Pfam domain sequences (release 21.0) using the blastx algorithm (E-value < 1e-10) [23]. Similarities to ESTs from libraries derived form xylem and/or cambium of Pinus, Picea, Poplar and Japanese cedar were determined with the tBLASTx program. We used Pinus Gene Index release 6.0 (PGI_libraries PHJ, PHM, ONA, PJD, ERF, 2NV, CJQ, 11 F, 0TU, PJQ, M7S, M7N, 9UQ, 72B, 0U0, 0TT-2, M7Q, M7R, M7P, M7O, PJT, PJM, ERE, CER, PHN, NIL, ERD, BTR, CCS, CJP, 8FB, PJR, ONB, OI1, CJS, ERB, 9NV, 5BN, 1RR, and 0TV), Spruce Gene Index release 2.0 (Sgi_libraries KH2, H5M, H5L, FKG, KGV, EOT, PHL, EOR, KH1, KH0, FH7, FKM, F7N, LCC, F7O, F7U, LCF, IQE, EOS, LCD, LCN, LCM, IQG, IQD, FH9, F7V, IQF, FKL, EOQ, and LCE), Poplar Gene Index release 3.0 (PplGI_libraries EA1, 9BN, BMF, G26, NIQ, EA2, ASV, NL3, FKA, DRG, F8V, F8D, 1CV, LRS, G22, G21, DRC, LRR, DRF, G27, and DQP) from The Gene Index Project website (http://compbio.dfci.harvard.edu/tgi/plant.html) [116], and the ForestGen database (inner bark and sapwood data) as EST databases [22].
PlnTFDB [30], a recently developed database of transcription factor families for 22 plant species, was used to identify putative transcription factors expressed during Japanese cedar wood formation. Blastx searches were performed on matches against A. thaliana and P. trichocarpa in the PlantTFDB with E-values < 1e-5.
The unique sequences were searched locally against a database of clusters of orthologous groups (COGs) from seven eukaryotic genomes [25]. The COGs are comprised of three databases containing orthologous proteins from at least three out of seven eukaryotic species (KOGs), proteins from two species (TWOGs), and lineage-specific expansion groups (LSEs). Sequences with E-values < 1e-5 were considered to have significant homology, and were classified following the KOG functional classification.
The sequences of ESTs have been submitted to the DNA Data Bank of Japan under accession numbers DC882454 through DC883482.
Microarray analysis
We built a custom microarray platform containing 60-mer oligonucleotide probes designed based on 14,612 isotigs (probes to 4 isotigs could be not designed) from all isotigsin proprietary NGS data and 3,470 EST sequences from the “sapwood” and “inner bark” categories (including a full-length cDNA library) in the ForestGen database [22]. A set of 18,082 probes was selected and accommodated in the NimbleGen 4 × 72 K array format (Roche-Nimblegen Inc., Waldkraiburg, Germany), which can examine the expression levels of up to 20,000 genes for four samples at the same time. Therefore, in this format, 18,082 probes were accommodated at least in triplicate in our custom array. For microarray analysis of five sampling dates, we used four biological replicates and three technical replicates for each sample (Additional file 1: Figure S1). Total RNA was extracted with a Plant RNeasy Mini Kit, and DNase was treated in-column with an RNase-Free DNase set (Qiagen). The A260/A280 ratios of RNA samples used for hybridization ranged from 1.7 to 2.0. An Agilent 2100 Bioanalyzer analyzed the integrity of RNA samples. RNA integrity values of samples used for hybridization ranged from 8.1 to 10.0. Double-stranded cDNA was synthesized using a SuperScript double-stranded cDNA synthesis kit (Invitrogen, Carlsbad, CA, USA) with random 6-mers following the manufacturer’s protocol. Cy3 labeling and hybridization were performed by NimbleGen using standard procedures. Labeled and hybridized slides were scanned using a NimbleGen MS 200 microarray scanner to generate paired files.
Because there were three or four spots for each target, the paired files contained redundant signal intensities for all probes. We took medians as representing intensities to avoid the effect of outliers, and loaded them into Subio platform software (Subio Inc., http://www.subio.jp) [117]. Intensity values were normalized at the 75th percentile, and then transformed into log2 ratios based on the average of the 60 samples, which were composed of 5 time points with 12 replicates each. The data presented in this study have been deposited in NCBI’s Gene Expression Omnibus and are accessible through GEO Series access number GSE53034.
Of the total 18,082 target genes, 748 with raw signal intensities not exceeding 1,000 in any samples were filtered out. We calculated the averages of log2 ratios at each time point, and excluded an additional 6,273 genes with expression levels hardly varying over time (between −0.5 and 0.5). We tested the 11,061 genes by ANOVA (p < 0.05 and BH-FDR < 0.2) to extract 10,380 genes with expression levels that varied for at least one time point. Hierarchical clustering (unweighted pair group method with arithmetic mean, Pearson correlation) was used to identify groups of co-expressed genes. We extracted clusters from tree nodes (Figure 5). We additionally created trees with gene sets manually selected based on biological knowledge.
Validation of quantitative RT-PCR
Independent verification of microarray results was carried out by qRT-PCR analysis using total RNA from the cambium region tissues used for microarray experiments. Total RNA (500 ng) was reverse-transcribed using the PrimeScript II 1st strand cDNA synthesis kit (Takara Bio, Otsu, Shiga, Japan) with random 6-mers following the manufacturer’s instructions. The resulting first-strand cDNA was diluted 1:5 in water before real-time PCR. Primers were designed using Primer Express software ver. 3.0 (Applied Biosystems, Foster City, CA, USA), with a melting temperature (Tm) between 60 and 65°C, and produced amplicons between 100 and 250 bp. Specific primer pairs were designed for each gene: Phenylalanine ammonia-lyase (PAL) (isotig 10873: forward 5′-GACCCAGGACGGGAAAGAG-3′, reverse 5′-TAGGCTGGAGTTCAAACGGTTT-3′); 4-Coumarate:CoA ligase (4CL) (isotig 04988: forward 5′-CAGTCGTCGCCAACTATGACA-3′, reverse 5′-ACGGCATCTTCCAGGTCCTT-3′) Cinnamate-4-hydroxylase (C4H) (isotig 09462: forward 5′-CGTTGAGAAGCTGCCGTATCT-3′, reverse 5′-CGTCAAGGGAGGCTTCTTCA-3′); Hydroxycinnamoyl-CoA shikimate/quinate hydroxycinnamoyl transferase (HCT) (isotig 10178: forward 5′-GCCCATCCATGATGCAGATT-3′, reverse 5′-GACTGGGCAAAATGAAACCAA-3′); p-Coumarate-3-hydroxylase (C3H) (isotig 02271: forward 5′-TCACATGGACCCCTCCTGAA-3′, reverse 5′-CGGTAGAGATGCTCAGGCAAT-3′); Caffeoyl-CoA O-methyltransferase; Cinnamyl alcohol dehydrogenase (CCoAOMT) (isotig 10196: forward 5′-ACTGCAGAGGCTTCCAAGGA-3′, reverse 5′-TCGCTCTGAAGGAGACTCTTGTG-3′); Cinnamoyl-CoA reductase (CCR) (isotig 05079: forward 5′-CAGGAGCGGGAGGATTTATTG-3′, reverse 5′-CCTCTGGATTGCGAACTGTTC-3′); Cinnamyl alcohol dehydrogenase (CAD)(isotig 02638: forward 5′-GCAGAGGCAGGCAAGAGATG-3′, reverse 5′-AGTCACATGATGCCCAAATGC-3′); Cellulose synthase (Ces) (isotig 08498: forward 5′-CATGGCCTGGGAACAACACT-3′, reverse 5′-ATGCGAGGCAGTTCGTTACC-3′); Sucrose synthase (Sus) (isotig 12351: forward 5′-ACGACTGTTCTTGGCAAACCAT-3′, reverse 5′-ATTGAGCGACCGGAACAAAC-3′); α-Tubulin (Tub α) (isotig 02753: forward 5′-CATCCTTGGGCACAACATCTC-3′, reverse 5′-TGCCTTTGAGCCTTCTTCCAT-3′); βTubulin (Tub β) (isotig 13384: forward 5′-TACACTGGTGAGGGCATGGA-3′, reverse 5′-GCATCCTCATCCGCAGTTG-3′); and the endogenous control Ubiquitin (UBQ) (forward 5′-CGTTAAAGCCAAGATCCAGGACAA-3′, reverse 5′-TCCATCCTCAAGCTGTTTCCCA-3′). For each sample, triplicate quantitative PCR assays were performed using Power SYBR Green PCR master mix (Applied Biosystems) with ROX reference dye according to the manufacturer’s protocol. Amplification was carried out with a StepOnePlus system (Applied Biosystems). After an initial 10-min activation step at 95°C, 40 cycles (95°C for 15 s and 60°C for 1 min) were performed, and a single fluorescent reading was obtained after each cycle immediately following the annealing/elongation step at 60°C. Preliminary quantitative PCR assays were performed to evaluate primer pair efficiency and absence of genomic DNA contamination using a negative control. A melting curve analysis was performed at the end of cycling to ensure amplification of a single product. For relative quantification and comparisons, we used the delta-delta-Ct method with Ubiquitin as the normalization internal control gene.
Notes
Declarations
Acknowledgements
We thank Dr. Mine Nose for providing us with the endogenous control primer for qRT-PCR. This work was supported by grants from the Japan Society for the Promotion of Science Grant-in-Aid for Scientific Research (number 24380098), the Program for Promotion of Basic and Applied Researches for Innovations in Bio-oriented Industry, the Forestry and Forest Products Research Institute (number 201004), and the project “Development of mitigation and adaptation techniques to global warming in the sectors of agriculture, forestry, and fisheries” financed by the Ministry of Agriculture, Forestry and Fisheries of Japan.
Authors’ Affiliations
References
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