Biofuel and energy crops: high-yield Saccharinae take center stage in the post-genomics era
© BioMed Central Ltd 2013
Published: 27 June 2013
The Saccharinae, especially sugarcane, Miscanthus and sorghum, present remarkable characteristics for bioenergy production. Biotechnology of these plants will be important for a sustainable feedstock supply. Herein, we review knowledge useful for their improvement and synergies gained by their parallel study.
Biofuels and sustainability
The replacement of fossil fuels by biofuels is an ongoing effort in many countries. With decreasing oil reserves and increasing fossil fuel prices, bioenergy is a promising alternative. Advantages of biofuels can include a positive energy balance, reduction of greenhouse gas emissions and indirect effects, such as rural development. Studies based on life-cycle analysis conclude that when ethanol from sugarcane is used to replace fossil fuels in transportation, a substantial reduction in net greenhouse gas emissions may result (from 80% to greater than 100% savings ). Biomass can also be used to generate electricity, with electric vehicles presenting several advantages over combustion engines. Wood, cellulose and biofuel generation of electricity and stationary generation of energy can be very efficient and are also being implemented as options. In the last 5 years we have seen a 109% increase in global biofuel production. World projections provided by the Organisation for Economic Co-operation and Development (OECD)/Food and Agriculture Organization (FAO) indicate further increases in bioethanol and biodiesel production from the present 140 billion liters to 221 billion liters in 2021, corresponding to an additional 60% increase.
Increased biofuel production, and the associated increase in production of energy feedstocks, raises sustainability concerns over issues such as changes in land use, competition between energy crops and food and feed crops, and impacts on ecosystem services, including soil and water resources. Mandates in several countries to substitute gasoline for bioethanol require a substantial contribution from advanced fuels (sugar-derived and/or lignocellulosic bioethanol) to guarantee a reduction of greenhouse gas emissions.
Which plants are best suited to the requirements of future bioenergy feedstocks? To produce energy from plant-fixed C-bonds, crops should be high yielding, fast growing, with C-bonds that are easy to convert to useful forms, and require relatively small energy inputs for growth and harvest. To achieve sustainability, energy crops should not require extensive use of prime agricultural lands and they should have a low cost of energy production from biomass. Both the realities of agriculture in environments that are always heterogeneous and energy security require that feedstocks include a portfolio of diverse crops rather than merely a single crop.
The Saccharinae group: many energy crop traits combined
Within the Andropogoneae grasses, sugarcane (Saccharum) and Miscanthus belong to the Saccharinae subtribe. Sorghum has been considered a member of the Sorghinae subtribe, although more recently a good case has been made (that we will accept herein) for expanding the Saccharinae to include the Sorghinae .
Origin, production and method of bioenergy production of the Saccharinae plants
Center of diversity
South to temperate east Asia
Limited: Asia, Europe, USA
Extensive: Brazil, India, China, others
Extensive: USA, Africa, central America, south Asia
Starch (grain); sugar; cellulosic
Complementing the tropical adaptation of Saccharum, with most species native to eastern or southeastern Asia , its adaptability to continental Europe [11–13] shows the feasibility of producing Miscanthus in temperate latitudes (Table 1). Miscanthus × giganteus, a sterile, vegetatively propagated hybrid (2n = 3x = 57) believed to originate from crosses between tetraploid Miscanthus sacchariflorus and diploid Miscanthus sinensis , generally produces high yields, similar to (and in some cases better than) other biomass crops [8, 15]. Considerable leveraging of breeding, production and processing infrastructure might be gained by the close relationship of Miscanthus to Saccharum - thought to be the closest relatives of one another, and polyphyletic . Saccharum × Miscanthus hybrids ('Miscanes') have been used for sugarcane improvement [17–19], and also show promise as a highly productive cellulosic biomass crop.
Increased demand for limited fresh water, along with rising global temperatures and aridity, suggest that sustainable future biomass production will have to occur using little or no irrigation, highlighting an important role of sorghum in a portfolio of bioenergy crops. One of the most drought tolerant of cereal crops thanks to its origins in Sudan and Ethiopia , the multifaceted history of sorghum improvement offers a wider range of genetic variations than found in many crops, exemplified by the fact that sorghum is one of the few crops suited to all proposed approaches for renewable fuel production (such as from starch, sugar, and/or cellulose; Table 1). About 30% of the US sorghum crop is presently used as feedstock in the grain-to-ethanol process, which has also been commercialized in India and China. The completely sequenced genome of sorghum, which has the further advantages of being relatively small and with minimal gene duplication , together with transformation potential, knowledge of cell wall composition and architecture and other features ( and references therein), make sorghum an important model for research concerning bioenergy grasses [22, 23].
Plants in the Andropogoneae use C4 photosynthesis (Box 1), which avoids photorespiration, leading to higher maximal photosynthetic energy conversion efficiency than the C3 pathway used by rice, wheat and many other grasses [5, 24], resulting in more biomass accumulation. In elevated CO2 conditions, the C4 grasses sugarcane , maize and sorghum  show better responses to drought stress than C3 grasses. Plants in the Saccharinae have some further advantages in comparison with other C4 grasses, such as maize. First, many routinely produce a 'ratoon' crop, regrowing after harvest and thus eliminating the need for replanting each year. Indeed, the Sorghum genus, with annual and perennial species that are genetically compatible, has become a botanical model for study of attributes related to perenniality [27–29]. Second, sugarcane and Miscanthus have lower nitrogen-input requirements [13, 30], and the latter can relocate some nutrients from aerial parts to the roots and/or rhizomes at the end of the growing season . Third, some reports show better photosynthetic features of Saccharinae plants than other Andropogoneae. Light interception by the leaves is higher in Miscanthus than in maize  and Miscanthus can sustain higher levels of CO2 assimilation than maize in lower temperatures . Sugarcane photosynthesis is enhanced in elevated CO2 in open-top chambers, increasing biomass productivity , which does not occur in maize grown in open-air elevation of CO2 . However, this finding is controversial since enclosure and open-air studies give different results for the same crop, and some authors argue that enclosed studies are not the best scenario to mimic future increases in CO2 concentration . Moreover, experiments with Miscanthus in ambient and open-air elevation of CO2 show no differences in yield .
Genomics meets biotechnology for the improvement of Saccharinae biofuel grasses
Improvements in sorghum are characteristic of many other major food and feed crops, and Miscanthus improvement is just beginning; examining sugarcane improvement therefore exemplifies the methods and approaches likely to be employed in biofuel grasses.
Sugarcane improvement efforts follow both molecular-assisted breeding and transgenic routes . S. officinarum is a plant with high sugar content in its stems but low productivity, and S. spontaneum has high tillering and biomass yield but low sugar accumulation. Modern sugarcane cultivars derive from a few crosses between S. officinarum and S. spontaneum and have been shown to be genetically very similar . Breeding programs have been able to increase yield and sucrose content by crossing cultivars but gains are becoming slimmer. To continue the improvement of yield it may be necessary to turn back to ancestral genotypes and broaden the genetic basis of crosses. S. spontaneum and S. robustum are also being used as parents, with the goal of designing a crop more amenable for cellulosic biofuel production, with increased stress tolerance and increased yield but less emphasis on stalk sugar concentration, the so-called 'energy cane'. World collections of Saccharum germplasm are held in Florida  and India , which keep ancestral genotypes and cultivars, and many private collections are also kept and used for crosses in specific breeding programs. Each world collection has over 1,500 accessions of ancestral genotypes, most of them S. officinarum (about 750), S. spontaneum (about 600) and S. robustum (about 130), and 500 to 1,000 hybrids or cultivars. Sorghum, like sugarcane, has large germplasm collections held by the US National Plant Germplasm System and at the International Crops Research Institute for the Semi-Arid Tropics (ICRISAT, the CGIAR center with a sorghum improvement mandate). Only a few small Miscanthus collections are held publicly, but several private collections associated with breeding programs are similar in size to the Saccharum collections.
Crosses between members of the Saccharinae are viable. In fact, sugarcane has been crossed to both Miscanthus and sorghum, generating viable progenies, and the strategy has been used to incorporate cold and drought resistance traits from Miscanthus into sugarcane .
The transformation of sugarcane is becoming an interesting and growing field. Methods for transformation are already established with efforts aimed mostly at sugar yield and quality [44–46], disease resistance [47, 48], and the use of sugarcane as a biofactory to produce high-value bioproducts [49, 50]. For biofuel production, some approaches show interesting results, with lower biomass recalcitrance  and expression and accumulation of microbial cellulolytic enzymes in sugarcane leaves  to improve biomass hydrolysis. The most widely used promoters are the constitutive CaMV 35S and maize ubi1, but sugarcane promoters have already been used or characterized, including tissue-specific [46, 47] and responsive promoters . However, sugarcane transformation is not a trivial task since problems such as transgene silencing frequently occur ([40, 54] and references therein). Sorghum transformation is also routine (although at lower efficiency than in some crops ), and Miscanthus transformation methods have been established .
Advantages of a reference genome
For both molecular-assisted and transgenic strategies outlined above, the availability of a reference genome sequence is highly desirable, as well as the definition of the complete complement of genes and proteins. For the Saccharinae, the relatively small (740 Mb) and diploid genome of sorghum, which has not experienced genome duplication in about 70 million years , has become the best reference for genomics and transcriptomics in sugarcane . Nonetheless, the sugarcane genome itself is being sequenced using a combination of approaches. In a first phase, researchers are sequencing bacterial artificial chromosomes (BACs) combined with whole-genome shot-gun sequencing to produce a reference genome . Currently, three sugarcane BAC libraries are available; from variety R570 , selfed progenies of R570  and SP80-3280 . The two former libraries have 103,000 to 110,000 clones comprising about 12 times coverage of the basic genome complement but only about 1.3 to 1.4 times coverage of the individual alleles. The latter library has about 36,000 clones, and all three have inserts of about 125 to 130 kb. BAC sequencing has enabled research to deduce synteny and collinearity of much of the sugarcane genome with other grasses, especially sorghum, particularly in genic regions [61–63]. Unaligned regions between sorghum and sugarcane genomes are largely repetitive , enriched in transposon-related sequences [61, 63]. Consistent with several genetic mapping efforts, the sequencing of BAC clones revealed high levels of gene structure/sequence conservation and collinearity among hom(oe)ologous haplotypes of the sugarcane genome , and several putative sugarcane-specific genes/sequences [61–63]. Groups from Australia, Brazil, France, South Africa and the USA are advancing these efforts in genome sequencing, increasing the number of BACs sequenced and producing shot-gun data of several cultivars. It is expected that reference genome sequences will be made available for both cultivars and ancestral genotypes  and, to that end, researchers are developing statistical models using SNPs where homology groups with any ploidy level may be estimated . This will be essential to obtain a saturated genetic map of the sugarcane genome that may aid genome assembly. The greatest challenge that distinguishes the sequencing of Saccharum and Miscanthus from the more tractable genomes of sorghum and other cereal models is large physical size (approximately 10 Gb) and large copy numbers of even 'low-copy' elements (8 to 12 in sugarcane; 4 to 6 in Miscanthus). During assembly of such genomes, many closely related alleles 'collapse' into single gene/element models that fail to capture allelic and perhaps also paralogous diversity within even a single genotype. The sorghum genome will greatly help in the assembly, but around 20% of the sugarcane expression sequence tags (ESTs) from the SUCEST project  appear to be specific to sugarcane, since they do not match sorghum, Miscanthus, maize, rice or Brachypodium , requiring other strategies in the assembly. Linkage maps based on molecular markers have shown synteny and collinearity of sorghum and sugarcane genomes, but are complicated to make in sugarcane due to the polyploidy and absence of inbred lines ( and references therein). This problem was partly overcome with the use of single-dose markers , which segregate in a 1:1 ratio in the gametes of a heterozygous genotype, and account for approximately 70% of polymorphic loci in sugarcane . However, among 20 to 30 linkage maps based on a few thousand markers available for sugarcane ([71, 72] and references therein), it remains true that only 33% to 60% of the sugarcane genome is represented on these maps . A recent development that may help breeders in marker-assisted selection efforts has been the development of an algorithm and software (ONEMAP) for constructing linkage maps of outcrossing plant species that has been successfully applied to sugarcane . Enriched mapping of DNA polymorphisms that also provide for deconvolution of closely related sequences may also aid in assembly of such highly polyploid genomes.
Summary of the microarray data available for sugarcane and Sorghum
No. of samples
Sugarcane ESTs nylon arrays I
Plantlet samples exposed to cold for up to 48 h
Saccharum hybrid cv.SP80-3280
SUCAST Sugarcane 2208 v1.0 (cDNA microarray)
Roots from six plants harvested 6, 12, 24 and 48 h after exposure to phosphate starvation
Saccharum hybrid cv.SP80-3280
Response to herbivory by Diatraea saccharalis
Response to N2-fixing endophytic bacteria association
Saccharum hybrid cv.SP70-1143
Leaves collected 24, 72 and 120 h after exposure to drought conditions for the control and experimental groups
Saccharum hybrid cv.SP90-1638
SUCAST 1920v3 (cDNA microarray)
The abundance of transcripts among six different sugarcane tissues (flowers, roots, leaves, lateral buds, 1st and 4th internodes)
Saccharum hybrid cv.SP80-3280
Leaves from sugarcane population segregated in relation to high and low brix
Affymetrix Sugarcane Genome Array
Leaves of sugarcane in response to sugar accumulation in meristem, internodes 1 to 3, internode 8, internode 20
Saccharum hybrid cv.Q117
Cold-girdles were attached to sugarcane leaves (n = 4) for a period of 56 h prior to harvest
Saccharum hybrid cv.N19
SUCEST-FUN Agilent 44k (oligo array)
Leaves were collected 24, 72 and 120 h after exposure to drought conditions for the control and experimental groups
Saccharum hybrid cv.SP90-1638
Seedlings exposed to high salinity, osmotic stress, and ABA for 3 and 27 h
Seedlings of Sorghum bicolor L. Moench cv BTx623
Seedlings exposed to salicylic acid, methyl jasmonate, and the ethylene precursor aminocyclopropane for 3 and 27 h
Seedlings of S. bicolor L. Moench cv BTx623
cDNA glass slide
Herbivory with Schizaphis graminum
Seedlings of S. bicolor ATx399 _ RTx430
Herbivory with Schizaphis graminum
Seedlings of S. bicolor M627 and Tx7000
Sorghum Agilent 44k (oligo array)
Leaves were collected 24, 72 and 120 h after exposure to drought conditions for the control and experimental groups
Grain of S. bicolor L. sweet Keller cv BTx623
Summary of the high-throughput sequencing data available for sugarcane, Sorghum and Miscanthus
Record GEO/NCBI, SRA
No. of samples
Illumina Genome Analyzer IIx
sRNA and non-coding RNAs of sugarcane in response to drought stress
Saccharum hybrid (mixed)
Illumina Genome Analyzer IIx
Examination of small RNAs in the sugarcane leaves that match to sugarcane LTR-RTs
Saccharum hybrid cv. SP80-3280
Identification of small RNAs associated with auxiliary bud outgrowth
Saccharum hybrid cv. SP80-3280
Illumina Genome Analyzer IIx
Screening of small RNA transcriptome of sugarcane plants infected with Acidovorax avenae subsp. avenae after 7 days
Saccharum hybrid cv. SP70-1143
Identification of sugarcane microRNAs after exposure to pathogens and microorganisms
Saccharum hybrid cv. SP70-1143
Identification of microRNA differentially expressed under drought stress, correlation between two cultivars with different drought tolerance
Saccharum hybrid cv. RB867515, RB855536
Increase the understanding of the role of microRNAs in the complex regulation of drought stress in field-grown sugarcane
Saccharum hybrid cv. RB867515, RB855536
Illumina Genome Analyzer II
RNA-Seq of Sorghum bicolor 9-day seedlings in response to osmotic stress and abscisic acid
Illumina Genome Analyzer IIx
Comparative sequence analysis of plant small RNAs
Comparative sequence analysis of plant small RNAs from leaves, flowers and panicle tissues
Illumina Genome Analyzer II
Develop sequence resources of small RNAs from different Miscanthus × giganteus tissues (including leaves, flowers and rhizomes)
Miscanthus × giganteus
Illumina Genome Analyzer II
RNAseq from two Miscanthus sinensis to define single nucleotide variants and find simple sequence repeat markers for understanding genomic responses to tetraploidy and chromosome fusion
ESTs corresponding to SUCEST, SoGI, JGI, GenBank (as of 4 March 2013)
Number of ESTs
Number of ESTs not in SUCEST
Number of clusters
Number of singletons
Number of predicted proteins
Number of putative ortholog/paralog genes between sugarcane, other grasses and Arabidopsis
No. of proteins
No. of cane orthologs (pairwise species)
No. of orthologs (multiple species)
The sugarcane transcriptome has been studied using technologies, including cDNA macroarrays (nylon membranes), cDNA microarrays spotted onto glass slides, and oligonucleotide arrays either spotted or synthesized in situ. A summary of the available platforms, samples and related works for sugarcane and sorghum using array technologies is shown in Table 3 and has been reviewed recently [57, 68, 78, 85]. Sugarcane transcriptomics has identified genes associated with sucrose content, biotic and abiotic stresses, photosynthesis, carbon partitioning and roles of phytohormones and signaling pathways in adaptive responses. These studies also allowed for the identification of promoters that can be used to drive transgene components in a tissue-specific or controlled manner. Several other methods to study sugarcane expression profiles at a moderate scale have been used to confirm the expression patterns observed in large-scale transcript studies .
More recently, the use of oligoarrays has included studies on the regulation of antisense gene expression in sugarcane, pointing to a role for these transcripts in drought responses . Some years ago, serial analysis of gene expression (SAGE) in sugarcane revealed an unexpectedly high proportion of antisense transcripts and chimeric SAGE . High-throughput sequencing (Table 4) is useful for assessing transcriptomes, providing detailed information for transcript variants, particularly SNPs, assessment of the expression of hom(oe)ologous alleles in the polyploid genome, spliced isoforms and so on . Using this strategy, some sugarcane genes were characterized for SNP density and gene haplotypes across varieties . In recent studies, it has become apparent that small RNAs, particularly microRNAs, have important regulatory roles in sugarcane, playing a key role in development and responses to biotic and abiotic stresses [90–92]. Evidence suggests that long terminal repeat retrotransposon (LTR-RT) families may affect nearby genes by generating a diverse set of small RNAs that trigger gene-silencing mechanisms .
In contrast to sorghum and sugarcane, genomic and transcriptomic studies on Miscanthus are just beginning. The recent high-throughput sequencing of its genome and transcriptome identified the presence of repeats that are actively producing small RNAs , and the construction of a genetic map identified informative simple sequence repeats in sugarcane and a genome-wide duplication in Miscanthus relative to S. bicolor . These studies will increase the understanding of complex genomes .
The Saccharinae grasses sugarcane, Miscanthus and sorghum are promising and complementary elements of a portfolio of bioenergy feedstocks. As sustainability criteria take dominant roles in the commercialization of biomass sources, these plants are likely to contribute to provide cheap, reliable and politically viable options for bioenergy production. Biotechnology for these crops is less advanced than in food crops such as maize and rice, but it is progressing quickly. Many efforts are underway to define genes associated with traits of interest such as sucrose content, drought tolerance, yield and adaptation to climate changes, and much is known about genes and markers for the improvement of these crops. Breeding programs are improving germplasm collections and defining routes to speed up selection of progenies and choice of ideal parents for crossing. It is expected that prudent integration of conventional breeding methods with marker-assisted and transgenic options may increase the (currently slow) rates of yield improvement, decreasing the amount of land required for large-scale biofuel production, as well as the need for inputs such as water, herbicides and fertilizers to maintain economical levels of production. Finally, the transition to a more biobased economy may be expedited by the increased value of biobased chemicals that might be harvested from the production chain through the adoption of integrated biorefinery systems. Better understanding of and greater control over carbon partitioning in these plants may greatly increase the number of co-products, including bioethanol, biodiesel, biokerosene, bioplastics and bioelectricity to name a few.
Box 1. C4 photosynthesis
bacterial artificial chromosome
expressed sequence tag
serial analysis of gene expression
sugarcane assembled sequence
single nucleotide polymorphism.
GMS is a recipient of a CNPq productivity Fellowship. SSF and MYN Jr are supported by graduate fellowships from CNPq and CAPES, respectively. GMS is funded by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) for research on sugarcane genome sequencing and functional genomics. The Saccharinae research of AHP has been funded by the International Consortium for Sugarcane Biotechnology, US National Science Foundation, US Department of Energy, US Department of Agriculture, Consortium for Plant Biotechnology Research, and Mendel Biotechnology.
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