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Cotton genome: challenge into the polyploidy

December 2017
Science Bulletin 62(24)

December 2017
62(24)

DOI:10.1016/j.scib.2017.11.022

Authors:

Zhiwen Chen

Hainan Yazhou Bay Seed Laboratory

Junfeng Cao

Chinese Academy of Sciences

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Commentary

Cotton genome: challenge into the polyploidy

Zhi-Wen Chen

, Jun-Feng Cao

, Xiu-Fang Zhang

, Xiao-Xia Shangguan

, Ying-Bo Mao

, Ling-Jian Wang

Xiao-Ya Chen

a,b,

⇑

National Key Laboratory of Plant Molecular Genetics and National Center for Plant Gene Research, Institute of Plant Physiology and Ecology, Shanghai Institutes for

Biological Sciences, Chinese Academy of Sciences, Shanghai 200032, China

Plant Science Research Center, Shanghai Chenshan Botanical Garden, Shanghai Key Laboratory of Plant Functional Genomics and Resources, Shanghai 201602, China

Cottons are the most important ﬁber crops in the world. The cot-

ton genus Gossypium has 52 species, including seven allotetraploid

species and 45 diploids. Four species were domesticated and remain

as crops under cultivation today: the New World allopolyploid spe-

cies G. hirsutum and G. barbadense (2n= 52), and the Old World

diploid species G. arboreum and G. herbaceum (2n= 26). The primary

cultivated species is Upland cotton (G. hirsutum L.), which accounts

for more than 90% of global cotton ﬁber production.

With the rapid development of genome sequencing technolo-

gies, cotton research has advanced greatly in recent several years,

such that nuclear genome sequences have now been published for

the model diploids (D

-genome [1,2],A

-genome [3]), and for the

allopolyploids (AD

-G. hirsutum [4,5],AD

-G. barbadense [6]). In

fact, the majority of crops have at least one genome assembly in

the public database, generating a myriad of new data from plant

genomes which are not only incubating new insights into plant

and agricultural sciences, such as plant evolution and domestica-

tion, but also revolutionizing breeding programs.

Firstly, cotton genome sequences contribute to elucidation of

the mechanism of ﬁber development. Cotton ﬁbers are unusually

long, single-celled epidermal seed trichomes and a model for

plant cell growth. Despite being the most important biological

event, our understanding of the regulation of ﬁber cell initiation

and elongation remain limited. The tetraploid G. hirsutum genome

harbors 28 members of the HD-ZIP IV subfamily. Genetic evidence

showed that, among these GL2-type homeodomain-containing

transcription factors, GhHOX3 plays a pivotal role in controlling

ﬁber elongation, and its activity is regulated by the phytohormone

gibberellin [7].

With the facility of genome sequences, some studies tried to

reveal the mechanism underlying ﬁber development. For example,

phytosterol content as well as the campesterol:sitosterol ratio

inﬂuence cotton ﬁber development [8], and cotton GhMYB7 is pre-

dominantly expressed in developing ﬁber cells and regulates sec-

ondary cell wall biosynthesis in transgenic Arabidopsis [9].

Furthermore, variations of transposable elements (TEs) may have

played a role in cotton ﬁber cell development [10], apart from

being responsible for the divergence of genome sizes between

cotton species.

Secondly, these cotton genome references are available to the

genome-wide analysis and expression proﬁling of the speciﬁc gene

family, such as phospholipase D gene family in G. arboreum [11],

NAC transcription factors gene family in diploid Gossypium [12]

and a mass of secondary metabolites such as gossypol, the cotton

phytoalexins against pathogens and herbivores [6,13].

Development of new genomic platforms and release of diploid

and tetraploid cotton genome sequences have greatly facilitated

the GWAS studies to hunt for candidate genes of important traits

(lint yield and ﬁber quality traits). However, understanding the

molecular mechanisms of ﬁber development is often hindered by

the complexity of polyploidy. With the coming of the genomics

era, polyploidy is attracting great attention from plant scientists,

especially those of the crop ﬁeld.

Following whole genome duplication, duplicated genes gener-

ally have several possible fates: both copies may be retained for

dosage balance, one copy is retained and the other copy has

been lost, silenced, or diverged to gain new function (neofunc-

tionalization or subfunctionalization) [14]. Thus one of the

important features to emerge from polyploid is massive alter-

ations in gene expression and function. In every allopolyploid

species examined to date, some fractions of the duplicate gene

pairs (homoeologs) are expressed unequally, as proved in the

allopolyploid cotton genome with the features of asymmetrical

evolution [5]. This suite of unequally expressed genes may vary

among species, tissues, and even cells, and thus is a fundamental

feature of allopolyploids. The genomic and transcriptomic data,

in combination with modern technologies such as gene editing

[15], shall reshape future breeding approaches for supper cotton

cultivars.

Conﬂict of interest

The authors declare that they have no conﬂict of interest.

https://doi.org/10.1016/j.scib.2017.11.022

⇑

Corresponding author.

E-mail addresses: chenzw@sippe.ac.cn (Z.-W. Chen), caojunfeng@sibs.ac.cn

(J.-F. Cao), xfzhang1990@163.com (X.-F. Zhang), sgxx@sibs.ac.cn (X.-X. Shangguan),

ybmao@sibs.ac.cn (Y.-B. Mao), ljwang@sibs.ac.cn (L.-J. Wang), xychen@sibs.ac.cn

(X.-Y. Chen).

Science Bulletin 62 (2017) 1622–1623

Contents lists available at ScienceDirect

Science Bulletin

journal homepage: www.elsevier.com/locate/scib

Acknowledgments

The research was supported by Chinese Academy of Sciences

(XDB11030000), Ministry of Science and Technology of China

and Ministry of Agriculture of China (2013CB127000,

2016YFA0500800, 2016ZX08009001-009, 2016ZX08005001-001),

National Natural Science Foundation of China (31690092).

References

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Gossypium raimondii. Nat Genet 2012;44:1098–103.

[2] Paterson AH, Wendel JF, Gundlach H, et al. Repeated polyploidization of

Gossypium genomes and the evolution of spinnable cotton ﬁbres. Nature

2012;492:423–7.

[3] Li FG, Fan GY, Wang KB, et al. Genome sequence of the cultivated cotton

Gossypium arboreum. Nat Genet 2014;46:567–72.

[4] Li FG, Fan GY, Lu CR, et al. Genome sequence of cultivated upland cotton

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[6] Liu X, Zhao B, Zheng HJ, et al. Gossypium barbadense genome sequence provides

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[7] Shan CM, Shangguan XX, Zhao B, et al. Control of cotton ﬁbre elongation by a

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[8] Deng SS, Wei T, Tan KL, et al. Phytosterol content and the campesterol:

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[9] Huang JF, Chen F, Wu SY, et al. Cotton GhMYB7 is predominantly expressed in

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gene editing in Arabidopsis thaliana. Sci Bull 2015;60:1332–47.

Z.-W. Chen et al. / Science Bulletin 62 (2017) 1622–1623 1623

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INT J MOL SCI

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Sorghum (Sorghum bicolor) is the fifth important cereal and an industrial energy crop in the world. Growth Regulation Factors (GRFs) play an important role in response to environmental stress, however, the knowledge of GRFs relating to the pest resistance is lacking. Here, we identified 8 GRF genes harboring the typical QLQ (glutamine, leucine, glutamine) and WRC (tryptophan, arginine, cysteine) domains in Sorghum, which could be classified into 4 clades through phylogenetic analysis. The SbGRF genes express in most tissues, while more than half of them express at the highest level in inflorescence. To further investigate their possible role in stress response, we analyzed the transcriptomics data. The results showed that SbGRFs could respond to the abiotic stresses including heat, salt and drought stress. Furthermore, combined the data with qRT-PCR, SbGRF1, 2, 4 and 7 were identified as dominant genes response to the aphid-induced stress. SSR markers close to these genes were also searched. Above all, we summarized the SbGRFs and provided their potential roles in aphid response.

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Background The cryptochromes (CRY) are specific blue light receptors of plants and animals, which play crucial roles in physiological processes of plant growth, development, and stress tolerance. Results In the present work, a systematic analysis of the CRY gene family was performed on twelve cotton species, resulting in 18, 17, 17, 17, and 17 CRYs identified in five alloteraploid cottons (Gossypium hirsutum, G. barbadense, G. tomentosum, G. mustelinum and G. darwinii), respectively, and five to nine CRY genes in the seven diploid species. Phylogenetic analysis of protein-coding sequences revealed that CRY genes from cottons and Arabidopsis thaliana could be classified into seven clades. Synteny analysis suggested that the homoeolog of G. hirsutum Gh_A02G0384 has undergone an evolutionary loss event in the other four allotetraploid cotton species. Cis-element analysis predicated the possible functions of CRY genes in G. hirsutum. RNA-seq data revealed that Gh_D09G2225, Gh_A09G2012 and Gh_A11G1040 had high expressions in fiber cells of different developmental states. In addition, the expression levels of one (Gh_A03G0120), 15 and nine GhCRY genes were down-regulated following the PEG, NaCl and high-temperature treatments, respectively. For the low-temperature treatment, five GhCRY genes were induced, and five were repressed. These results indicated that most GhCRY genes negatively regulate the abiotic stress treatments. Conclusion We report the structures, domains, divergence, synteny, and cis-elements analyses systematically of G. hirsutum CRY genes. Possible biological functions of GhCRY genes in differential tissues as well as in response to abiotic stress during the cotton plant life cycle were predicted.

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Cotton has a tremendous economic value worldwide due to its high-quality fiber, edible oil and protein contents. However, the intensifying scenario of human population expansion and global environmental changes demand a proportionate increase in cotton production. In the past, several successful attempts have been made by introgression of many quality- and yield-related traits into elite cotton cultivars through conventional breeding. However, those measures are time consuming due to the reliance on introgression of naturally-existing genetic variation through extensive backcrossing. Nonetheless, plant breeding can be accelerated through modern genome editing (GE) tools. Various GE techniques including zinc finger nucleases (ZFNs), transcription activator-like effector nucleases (TALENs), and clustered regularly interspaced palindromic repeats and CRISPR-associated proteins systems (CRISPR/Cas)-based approaches have been successfully employed for various crop plants. Among them, CRISPR/Cas-based approaches hold great GE potential due to their simplicity, competency and versatility. In cotton, this system can regulate the gene expression associated with quality traits, to circumscribe phytopathogens and/or to stack molecular traits at a desired locus. In gene stacking through site-specific endonucleases, the desired genes can be introduced in close proximity to a specific locus in the cotton genome with a low risk of segregation. However, such executions are tedious to achieve through classical breeding techniques. Moreover, through the CRISPR/Cas-based approaches, transgene-free cotton plants can easily be produced by selfing or backcrossing to meet the current genetically modified organisms (GMO) guidelines. In this chapter, we address the potential application of CRISPR/Cas-based approaches in available whole cotton genomes to sustain cotton productivity, and achieve genetic improvement, pathogen resistance and agronomic traits. Future prospects of GE applications in cotton breeding are also addressed.

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Determining the genetic rearrangement and domestication footprints in Gossypium hirsutum cultivars and primitive race genotypes are essential for effective gene conservation efforts and the development of advanced breeding molecular markers for marker-assisted breeding. In this study, 94 accessions representing the 7 primitive races of G hirsutum, along with 9 G hirsutum and 12 Gossypium barbadense cultivated accessions were evaluated. The genotyping-by-sequencing (GBS) approach was employed and 146 558 single nucleotide polymorphisms (SNP) were generated. Distinct SNP signatures were identified through the combination of selection scans and association analyses. Phylogenetic analyses were also conducted, and we concluded that the Latifolium, Richmondi, and Marie-Galante race accessions were more genetically related to the G hirsutum cultivars and tend to cluster together. Fifty-four outlier SNP loci were identified by selection-scan analysis, and 3 SNPs were located in genes related to the processes of plant responding to stress conditions and confirmed through further genome-wide signals of marker-phenotype association analysis, which indicate a clear selection signature for such trait. These results identified useful candidate gene locus for cotton breeding programs.

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Identification and Functional Characterization of Gh_D01G0514 (GhNAC072) Transcription Factor in Response to Drought Stress Tolerance in Cotton

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Cotton encounters long-term drought stress problems resulting in major yield losses. Transcription factors (TFs) plays an important role in response to biotic and abiotic stresses. The coexpression patterns of gene networks associated with drought stress tolerance were investigated using transcriptome profiles. Applying a weighted gene co-expression network analysis, we discovered a salmon module with 144 genes strongly linked to drought stress tolerance. Based on coexpression and RT-qPCR analysis GH_D01G0514 was selected as the candidate gene because of its consistent expression in response to drought stress in both leaves and roots. Moreover, coexpression network analysis also identifies it as a hub gene in both tissues. For validation of GH_D01G0514, Virus Induced Gene Silencing was performed and VIGS plants showed significantly higher excised leaf water loss and ion leakage, while lower relative water and chlorophyll contents as compared to WT (Wild type) and positive control plants. Furthermore, the WT and positive control seedlings showed higher in CAT and SOD, and low in Hydrogen peroxide and MDA enzymes than the VIGS plants. Gh_D01G0514 (GhNAC072) was localized in the nucleus and cytoplasm. Y2H assay demonstrates that Gh_D01G0514 has a potential of auto activation. It was observed that the Gh_D01G0514 was highly upregulated in both tissues based on RNA Seq and RT-qPCR analysis. Thus, we inferred that, the candidate gene might be responsible for drought stress tolerance in cotton. This finding adds significantly to the existing knowledge of drought stress tolerance in cotton and deep molecular analysis required to understand the molecular mechanisms underlying drought stress tolerance in cotton.

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Of the two cultivated species of allopolyploid cotton, Gossypium barbadense produces extra-long fibers for the production of superior textiles. We sequenced its genome (AD) 2 and performed a comparative analysis. We identified three bursts of retrotransposons from 20 million years ago (Mya) and a genome-wide uneven pseudogenization peak at 11-20 Mya, which likely contributed to genomic divergences. Among the 2,483 genes preferentially expressed in fiber, a cell elongation regulator, PRE1, is strikingly At biased and fiber specific, echoing the A-genome origin of spinnable fiber. The expansion of the PRE members implies a genetic factor that underlies fiber elongation. Mature cotton fiber consists of nearly pure cellulose. G. barbadense and G. hirsutum contain 29 and 30 cellulose synthase (CesA) genes, respectively; whereas most of these genes (>25) are expressed in fiber, genes for secondary cell wall biosynthesis exhibited a delayed and higher degree of up-regulation in G. barbadense compared with G. hirsutum, conferring an extended elongation stage and highly active secondary wall deposition during extra-long fiber development. The rapid diversification of sesquiterpene synthase genes in the gossypol pathway exemplifies the chemical diversity of lineage-specific secondary metabolites. The G. barbadense genome advances our understanding of allopolyploidy, which will help improve cotton fiber quality.

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Article

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The newly developed CRISPR (Clustered Regularly Interspaced Short Palindromic Repeats)/Cas (CRISPR-associated) system has emerged as an efficient tool for genome-editing, providing an alternative to classical mutagenesis and transgenic methods to study gene function and improve crop traits. CRISPR/Cas facilitates targeted gene editing through RNA-guided DNA cleavage followed by cellular DNA repair mechanisms that introduce sequence changes at the site of cleavage. Here we describe a detailed procedure for our previously developed and highly efficient CRISPR/Cas9 method that allows the generation of heritable-targeted gene mutations and corrections in Arabidopsis. This protocol describes the strategies and steps for the selection of targets, design of single-guide RNA (sgRNA), vector construction and analysis of transgenic lines. We also offer a method to target two loci simultaneously using vectors containing two different sgRNAs. The principles described in this protocol can be applied to other plant species to generate stably inherited DNA modifications. © 2015, Science China Press and Springer-Verlag Berlin Heidelberg.

Genome sequence of cultivated Upland cotton (Gossypium hirsutum TM-1) provides insights into genome evolution

Article

Full-text available

Apr 2015
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Gossypium hirsutum has proven difficult to sequence owing to its complex allotetraploid (AtDt) genome. Here we produce a draft genome using 181-fold paired-end sequences assisted by fivefold BAC-to-BAC sequences and a high-resolution genetic map. In our assembly 88.5% of the 2,173-Mb scaffolds, which cover 89.6%∼96.7% of the AtDt genome, are anchored and oriented to 26 pseudochromosomes. Comparison of this G. hirsutum AtDt genome with the already sequenced diploid Gossypium arboreum (AA) and Gossypium raimondii (DD) genomes revealed conserved gene order. Repeated sequences account for 67.2% of the AtDt genome, and transposable elements (TEs) originating from Dt seem more active than from At. Reduction in the AtDt genome size occurred after allopolyploidization. The A or At genome may have undergone positive selection for fiber traits. Concerted evolution of different regulatory mechanisms for Cellulose synthase (CesA) and 1-Aminocyclopropane-1-carboxylic acid oxidase1 and 3 (ACO1,3) may be important for enhanced fiber production in G. hirsutum.

Cotton GhMYB7 is predominantly expressed in developing fibers and regulates secondary cell wall biosynthesis in transgenic Arabidopsis

Article

Jan 2016

The secondary cell wall in mature cotton fibers contains over 90% cellulose with low quantities of xylan and lignin. However, little is known regarding the regulation of secondary cell wall biosynthesis in cotton fibers. In this study, we characterized an R2R3-MYB transcription factor, GhMYB7, in cotton. GhMYB7 is expressed at a high level in developing fibers and encodes a MYB protein that is targeted to the cell nucleus and has transcriptional activation activity. Ectopic expression of GhMYB7 in Arabidopsis resulted in small, curled, dark green leaves and also led to shorter inflorescence stems. A cross-sectional assay of basal stems revealed that cell wall thickness of vessels and interfascicular fibers was higher in transgenic lines overexpressing GhMYB7 than in the wild type. Constitutive expression of GhMYB7 in Arabidopsis activated the expression of a suite of secondary cell wall biosynthesis-related genes (including some secondary cell wall-associated transcription factors), leading to the ectopic deposition of cellulose and lignin. The ectopic deposition of secondary cell walls may have been initiated before the cessation of cell expansion. Moreover, GhMYB7 was capable of binding to the promoter regions of AtSND1 and AtCesA4, suggesting that GhMYB7 may function upstream of NAC transcription factors. Collectively, these findings suggest that GhMYB7 is a potential transcriptional activator, which may participate in regulating secondary cell wall biosynthesis of cotton fibers.

Gossypol: phytoalexin of cotton

Article

Jan 2016

Sesquiterpenoids are a class of 15-carbon secondary metabolites that play diverse roles in plant adaptation to environment. Cotton plants accumulate a large amount of sesquiterpene aldehydes (including gossypol) as phytoalexins against pathogens and herbivores. They are stored in pigment glands of aerial organs and in epidermal layers of roots. Several enzymes of gossypol biosynthesis pathway have been characterized, including 3-hydroxy-3-methylglutaryl coenzyme A reductase (HMGR) and farnesyl diphosphate synthase (FPS) that catalyze the formation of the precursor farnesyl diphosphate (FPP), (+)-δ-cadinene synthase (CDN) which is the first enzyme committed to gossypol biosynthesis, and the downstream enzymes of CYP706B1 and methyltransferase. Expressions of these genes are tightly regulated during cotton plants development and induced by jasmonate and fungi elicitors. The transcription factor GaWRKY1 has been shown to be involved in gossypol pathway regulation. Recent development of new genomic platforms and methods and releases of diploid and tetraploid cotton genome sequences will greatly facilitate the elucidation of gossypol biosynthetic pathway and its regulation.

Phytosterol content and the campesterol:sitosterol ratio influence cotton fiber development: role of phytosterols in cell elongation

Article

Jan 2016

Phytosterols play an important role in plant growth and development, including cell division, cell elongation, embryogenesis, cellulose biosynthesis, and cell wall formation. Cotton fiber, which undergoes synchronous cell elongation and a large amount of cellulose synthesis, is an ideal model for the study of plant cell elongation and cell wall biogenesis. The role of phytosterols in fiber growth was investigated by treating the fibers with tridemorph, a sterol biosynthetic inhibitor. The inhibition of phytosterol biosynthesis resulted in an apparent suppression of fiber elongation in vitro or in planta. The determination of phytosterol quantity indicated that sitosterol and campesterol were the major phytosterols in cotton fibers; moreover, higher concentrations of these phytosterols were observed during the period of rapid elongation of fibers. Furthermore, the decrease and increase in campesterol:sitosterol ratio was associated with the increase and decease in speed of elongation, respectively, during the elongation stage. The increase in the ratio was associated with the transition from cell elongation to secondary cell wall synthesis. In addition, a number of phytosterol biosynthetic genes were down-regulated in the short fibers of ligon lintless-1 mutant, compared to its near-isogenic wild-type TM-1. These results demonstrated that phytosterols play a crucial role in cotton fiber development, and particularly in fiber elongation.

Comprehensive analysis of NAC transcription factors in diploid Gossypium: sequence conservation and expression analysis uncover their roles during fiber development

Article

Jan 2016

Determining how function evolves following gene duplication is necessary for understanding gene expansion. Transcription factors (TFs) are a class of proteins that regulate gene expression by binding to specific cis-acting elements in the promoters of target genes, subsequently activating or repressing their transcription. In the present study, we systematically examined the functional diversification of the NAC transcription factor (NAC-TFs) family by analyzing their chromosomal location, structure, phylogeny, and expression pattern in Gossypium raimondii (Gr) and G. arboreum (Ga). The 145 and 141 NAC genes identified in the Gr and Ga genomes, respectively, were annotated and divided into 18 subfamilies, which showed distinct divergence in gene structure and expression patterns during fiber development. In addition, when the functional parameters were examined, clear divergence was observed within tandem clusters, which suggested that subfunctionalization had occurred among duplicate genes. The expression patterns of homologous gene pairs also changed, suggestive of the diversification of gene function during the evolution of diploid cotton. These findings provide insights into the mechanisms underlying the functional differentiation of duplicated NAC-TFs genes in two diploid cotton species.

Genome-wide analysis and expression profiling of the phospholipase D gene family in Gossypium arboreum

Article

Dec 2015
Sci China Life Sci

The plant phospholipase D (PLD) plays versatile functions in multiple aspects of plant growth, development, and stress responses. However, until now, our knowledge concerning the PLD gene family members and their expression patterns in cotton has been limited. In this study, we performed for the first time the genome-wide analysis and expression profiling of PLD gene family in Gossypium arboretum, and finally, a total of 19 non-redundant PLD genes (GaPLDs) were identified. Based on the phylogenetic analysis, they were divided into six well-supported clades (α, β/γ, δ, ε, ζ and φ). Most of the GaPLD genes within the same clade showed the similar exon-intron organization and highly conserved motif structures. Additionally, the chromosomal distribution pattern revealed that GaPLD genes were unevenly distributed across 10 of the 13 cotton chromosomes. Segmental duplication is the major contributor to the expansion of GaPLD gene family and estimated to have occurred from 19.61 to 20.44 million years ago when a recent large-scale genome duplication occurred in cotton. Moreover, the expression profiling provides the functional divergence of GaPLD genes in cotton and provides some new light on the molecular mechanisms of GaPLDα1 and GaPLDδ2 in fiber development.

Transposable elements play an important role during cotton genome evolution and fiber cell development

Article

Dec 2015
Sci China Life Sci

Transposable elements (TEs) usually occupy largest fractions of plant genome and are also the most variable part of the structure. Although traditionally it is hallmarked as "junk and selfish DNA", today more and more evidence points out TE's participation in gene regulations including gene mutation, duplication, movement and novel gene creation via genetic and epigenetic mechanisms. The recently sequenced genomes of diploid cottons Gossypium arboreum (AA) and Gossypium raimondii (DD) together with their allotetraploid progeny Gossypium hirsutum (AtAtDtDt) provides a unique opportunity to compare genome variations in the Gossypium genus and to analyze the functions of TEs during its evolution. TEs accounted for 57%, 68.5% and 67.2%, respectively in DD, AA and AtAtDtDt genomes. The 1,694 Mb A-genome was found to harbor more LTR(long terminal repeat)-type retrotransposons that made cardinal contributions to the twofold increase in its genome size after evolution from the 775.2 Mb D-genome. Although the 2,173 Mb AtAtDtDt genome showed similar TE content to the A-genome, the total numbers of LTR-gypsy and LTR-copia type TEs varied significantly between these two genomes. Considering their roles on rewiring gene regulatory networks, we believe that TEs may somehow be involved in cotton fiber cell development. Indeed, the insertion or deletion of different TEs in the upstream region of two important transcription factor genes in At or Dt subgenomes resulted in qualitative differences in target gene expression. We suggest that our findings may open a window for improving cotton agronomic traits by editing TE activities.

The wondrous cycles of polyploidy in plants

Article

Oct 2015
AM J BOT

Jonathan F. Wendel

Cotton genome: challenge into the polyploidy

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