Wheat functional genomics research in China:A decade of development

1.Introduction

In the past decade we witnessed a revolutionary development of wheat genomics and functional genomics,thanks to the development of next generation sequencing(NSG)technology.Wheat,as one of the most important crops in China and the world and with a huge,repetitive,and polyploid genome,was unconquerable in the past and is now catching up with other crops due to the availability of an increasing number of resources and platforms.

Wheat researchers in China have worked unostentatiously during the last decade after The National High Technology Research and Development Program of China first set up the wheat functional genomics program in 2005.Since then many papers on wheat were published in a wide range of international journals demonstrating significant progress in wheat functional genomics.

At such an exciting moment it is timely to publish a special issue of The Crop Journal on wheat functional genomics to showcase the achievements of Chinese wheat researchers to the world crop community.Here,we compiled nine review papers and one research article.The aim of this special issue is to overview major progress in wheat functional genomics,especially in China.We also predict the future direction of wheat functional genomics research.We must acknowledge the landmark contributions of the international wheat research community,without which it would have been much harder for Chinese researchers to reach their goals.The publication of this special issue is therefore to acquaint our colleagues both within and outside China with the work conducted by Chinese wheat scientists and to promote further international collaborations in wheat functional genomics research.The following is a brief introduction to these review articles.Moreover,a number of important achievements in wheat functional genomics studies that are not included in this issue are also highlighted.

2.Pioneering work in wheat genome sequencing and analysis

Jia et al.[1]highlight currently available tools and methodologies for wheat functional genomics research that were developed in the era of NGS technology.These range from the concerted international effort in generating multiple reference genomes to novel strategies to attain genome-wide genetic variation; from mutant population generation to NGS-supported gene cloning and functional characterization.These resources provide the necessary foundation for wheat research by bridging the gap between genotype and phenotype and greatly support genomics-assisted selection and breeding of elite varieties.Shi and Ling[2]then provide a comprehensive overview on the development of wheat genome sequencing that occurred in the last five years.Diploid donor species,such as Triticum urartu,the AA genome donor and Aegilops tauschii,the DD genome donor,were first sequenced by two groups led by Chinese Scientists[3,4],accompanied by the simultaneous acquisition of a shotgun-derived draft sequence of common wheat variety Chinese Spring[5].Over the next few years,a series of wheat genome sequences were published by the International Wheat Genome Sequencing Consortium(IWGSC)[6,7].The recent publication of a high quality wild em mer genome[8]permits further improvement of both the diploid and hexaploid wheat genome sequences.The availability of three levels of wheat genome sequences provides a long needed stepping-stone to conduct functional genomics researches in wheat.

3.A leap in transformation efficiency for wheat genome editing

One of the key developments for wheat functional genomics is the breakthrough in wheat plant transformation.The mysterious and patented technology that was developed by the Japanese Tobacco Institute has been transferred to other counties such as China,providing critical support for functional characterization of wheat genes.Wang et al.[9]review recent progress in wheat transformation that greatly expedited the application of genome editing technology in this important crop.Together with other platforms,such as ex on sequenced TILLING libraries[10],the functions of a large number of genes responsible for important agronomic traits will be identified in the foreseeable future.Together with recent progress in plant genome editing technology,these authors discuss possibilities to further increase transformation efficiency and to generate publicly acceptable,biotech-nologically engineered wheat varieties.

4.Understanding molecular mechanisms of wheat response to heat and salt stresses

Environmental changes are major factors affecting wheat yield.In this special issue,two review articles report recent studies on heat tolerance and salt tolerance in wheat.With increasing global warming,the weather has become less predictable,especially during the grain development and ripening period when hot,dry winds may cause significant yield losses.Ni et al.[11]review recent progress in understanding the molecular mechanisms of heat tolerance and related genetic improvement in wheat.They introduce recent works in identification of heat-tolerance QTL on different chromosomes and heat responsive genes/proteins using genome-wide analysis.Hormones,especially ABA and ethylene,and epigenetics are new factors and mechanisms involved in regulation of heat tolerance in wheat[11].On the other hand,saline land represents a large area that can be utilized for agriculture using salt tolerant crops.Study of the molecular mechanisms of salt tolerance in wheat should greatly help in breeding salt tolerant wheat varieties that can be grown on large areas of saline coastal land in China as well as many other locations in the world.Wang and Xia[12]overview current understanding of the major physiological processes associated with salt tolerance and the genes controlling them.They particularly focus on high-affinity potassium transporter(HKT)genes in enhancing salt tolerance in wheat.They also report studies to link maintenance of reactive oxygen species(ROS)homeostasis and salt tolerance through comprehensive studies on a wheat introgression line.The authors summarize the most recent progress in omics investigations,and new research strategies to uncover the mechanisms underlying salt tolerance[12].

5.Continuous effort to understand mechanisms underlying disease resistance

The arms race between crops and pathogens is an ongoing subject in biology.Fusarium head blight(FHB)or scab caused by Fusarium graminearum is a major threat to wheat production in China and elsewhere.This special issue features a review from Dr.Zhengqiang Ma's laboratory at Nanjing Agricultural University where there has been a long and arduous effort covering almost twenty years to understand Fusarium head blight resistance in Chinese wheat landrace Wangshuibai.They present results on resistance QTL identification, candidate functional gene discovery, and marker-assisted improvement of FHB resistant varieties.Although one gene effective in FHB resistance has been cloned[13],the underlying molecular mechanism of resistance to this devastating disease is still controversial and far from being fully understood[14].

6.An emerging genomics era for biotrophic pathogens in wheat

Obligate biotrophic fungi such as those that cause rust and powdery mildew diseases are major biotic constraints on wheat production in China as well as the world.The team led by Professor Zhengshen Kang at Northwest Agriculture and Forestry University is one of the leading groups in pathogenomics studies of wheat biotrophic fungi in the world.Here,Tang et al.[15]review recent progress in the application of next generation sequencing technology to achieve the genome sequences of wheat pathogens.The authors summarize recent genomics advances in understanding the biology and pathogenesis of biotrophic fungal pathogens attacking wheat both in China and in the world.Genomics advances in all three major rust pathogens–Puccinia striiformis f.sp.tritici(Pst),Puccinia graminis f.sp.tritici(Pgt),and Puccinia triticina(Pt)that cause stripe rust,stem rust and leaf rust,respectively,and Blumeria graminis f.sp.tritici(Bgt)that causes powdery mildew are introduced particularly in regard to their genome sequencing,avirulence gene cloning,effector discovery,and pathogenomics.New insights in biotrophic adaptation,pathogenicity mechanisms,and population dynamics of these fungi should assist in development of new strategies for breeding wheat varieties with durable resistance.Such knowledge is essential for wheat variety deployment in regard to year-to-year dynamics of wheat pathogen populations and hence better field management and yield.

7.Extensive genetic and genomics analyses of wheat grain qualities

Grain quality is central to food processing and nutritional value of wheat-based food products.It is a decisive factor for consumer acceptance and commercial value of wheat cultivars.Wang et al.[16]review recent progress in understanding molecular genetics and genomics mechanisms of wheat grain quality,particularly in regard to milling and end-use traits.The authors review multiple pubications by Chinese scientists to understand the relationships between grain hardness and milling traits and between gluten protein quality and end-use traits,especially the roles of the HMW-GS proteins,LMW-GS proteins,and gliadins,as well as the transcriptional regulation of those genes.The authors also introduce their effort to establish a mutation platform for systematic study of wheat grain quality[16].

8.Valuable breeding experience from the home town of Chinese Spring

The last review article in this special issue is about wheat breeding activities in the home-town of Chinese Spring,Chengdu,Sichuan.Breeding is not the focus of this issue,but Chinese Spring(CS)is special.CS was first made known to the world due to the life-time work of the American wheat cytogenetist,Dr.Ernie Sears,who developed several sets of CS-based aneuploid stocks that contributed to the establishment of a standard karyotype that allowed wheat researchers to analyze and manipulate the genome of wheat with unprecedented precision and efficiency[17,18].CS is the internationally chosen accession for a reference genome for the wheat community,with nearly all resources based upon it.Professor Deng-Cai Liu and colleagues from Sichuan Agricultural University [19] review the origin of the sister accession of CS known as Cheng-du-guang-tou and its role in local wheat breeding.This vivid story depicts the history of wheat breeding in Southwest China,from land races to synthetic wheat,and provides lessons for wheat breeders in China as well as the world.

Significant progress beyond this special issue

The above works are only the ones that could be sampled in one special issue. Many other contributions that are not included here should be mentioned. While wheat genomics is at its infancy, functional genomics in general continues to be pursued. Significant advances have been made in wheat flowering, nutrient up-take, polyploid formation, and genetic variation. Importantly, young scientists trained in model plants are joining the wheat community.

9.New discoveries in wheat vernalization,flowering,and inflorescence development

Vernalization is one of the most prominent features of wheat,a phenomenon that is of interest to nearly all plant biologists.A study by Dr.Kang Chong's laboratory at the Institute of Botany,Chinese Academy of Sciences(CAS),revealed a novel mechanism of control of TaVRN1 mRNA accumulation in response to prolonged cold sensing in wheat[20].TaVRN1 is an AP1 clade MADS-box transcription factor.The authors found that a jacalin lectin protein VER2 physically interacts with the RNA-binding protein TaGRP2,an interaction requiring O-GlcNAc modification on TaGRP2which gradually increases during vernalization.Interestingly,the interaction between VER2 and O-GlcNAc-TaGRP2 reduces TaGRP2 protein accumulation in the nucleus and/or promotes TaGRP2 dissociation from TaVRN1,leading to TaVRN1 mRNA accumulation.This novel mechanism is complementary to the epigenetic mechanism for vernalization and flowering that is well-known in other plants such as Arabidopsis.

Since most wheat varieties are winter or alternate types that flower in early spring,control of flowering time is critical for timely flowering and grain development and hence final yield.Zhao et al.[21]found that wheat micro RNA tae-miR408 targets the key circadian gene TIMING OF CAB EXPRESSION(TaTOC)and is involved in wheat flowering.That work indicated that tae-miR408 regulates wheat heading time by mediating TaTOC1expression,providing important new information on the mechanism underlying regulation of heading time in wheat.

Early inflorescence development is highly relevant to final grain number per spike and hence final yield potential.Feng et al.[22]at the Institute of Crop Science,CAAS,studied transcriptome profiles at four stages of early wheat reproductive development,from spikelet initiation to floral organ differentiation.They also sequenced the small RNA pools at these four stages and found conserved miRNA-mediated regulatory mechanisms in wheat inflorescence similar to those reported in model plants such as Arabidopsis[22].

Jiao and colleagues at the Institute of Genetics and Developmental Biology (IGDB), CAS, analyzed the transcriptomes of developing spikes in 90 wheat lines,74 landracesand 16 elitevarieties.In combination with coexpression network analysis,they inferred the identities of genes that may be related to spike complexity.A number of genes were further identified experimentally to be associated with inflorescence complexity[23].

10.Better understanding of genes responsible for nutrient uptake in wheat

The group led by Dr.Yiping Tong at IGDB,CAS,conducted interesting work related to wheat yield improvement by genetic regulation of nutrient utilization genes,including those involved in root meristem development[24],nitrate uptake related NAC genes[25,26]and NFYB genes[27].In order to study the role of auxin in wheat yield,Tong and colleagues performed genome-wide analysis to identify the tryptophan aminotransferase of Arabidopsis1/Tryptophan Aminotransferase-Related(TAA1/TAR)genes that function in the tryptophan-dependent pathway of auxin biosynthesis.Among 15 TaTAR genes identified using bioinformatics tools,genetic analysis showed that TaTAR2.1 was closely correlated with wheat grain yield.Knockdown of TaTAR2.1 caused vegetative and reproductive deficiencies,with impaired lateral root(LR)growth under both high-and low-N conditions.Overexpression of TaTAR2.1-3A,on the other hand,enhanced LR branching,plant height,spike number,grain yield,and aerial N accumulation under different N supply levels.These results indicate that wheat TaTAR genes are important for wheat growth and yield[28].

11.New Insights into the molecular mechanisms of wheat polyploidization

Common wheat is a product of hybridization between a tetraploid progenitor and a diploid one,followed by spontaneous chromosome doubling.This process is repeatable in the form of so called synthetic wheat and is introduced in the paper by Liu et al.[19].A number of studies have attempted to understand the molecular mechanisms underlying the process of polyploidization.The group of Professor Bao Liu at Northeast Normal University,Changchun,Jilin province,systematically studied genomic changes caused by chromosome alteration[29–31],genome interaction[32,33],and gene expression[34]after hybridization.Liu and co-workers studied heritable alterations in DNA methylation induced by whole-chromosome aneuploidy in wheat.Their results suggested that heritability of aneuploidy-generated, but aneuploidy-independent,phenotypic variation may have an epigenetic basis and that aneuploidy may have played an important and protracted role,probably via an epigenetic mechanism,in polyploid genome evolution[35].The roles of epigenetic modification on polyploid wheat genomes,espe-cially repetitive sequences and centromeres,were also reported by Dr.Fangpu Han's group at IGBD-CAS[36–39].

Interesting results for the effects of polyploidization on gene expression levels were reported by several groups,such as transcriptome asymmetry in synthetic and natural allotetraploid wheats[34].These studies suggest possible rules for differential contribution of the sub genomes derived from different progenitors in allohexaploid wheat[40–42].The findings that microRNAs seem to play broader roles than previously expected for growth rate and vigor may indicate broader functions of non-coding RNAs in wheat development as demonstrated by Feng et al.[22].

12.Identification of additional disease resistance genes in wheat

In addition to the effort to clone resistance genes for Fhb,there have been efforts to clone genes for resistance to other diseases.Besides the identification of serine/threonine kinase gene Stpk-V as a key component of powdery mildew resistance gene Pm21 that was introduced into wheat by distant hybridization from Dasypyrum villosum(Haynaldia villosa)[43],genes involved in resistance to take-all disease[44],Bipolaris sorokiniana[45],and Rhizoctonia cerealis[46,47]were also characterized.Engineering of wheat disease resistance genes by genome editing techniques such as TALENS and CRISPR/Cas9 were reviewed by Wang et al.in this special issue[9].

13.Establishment of a phenotyped Chinese wheat mini-core collection for genome-wide genetic variation study

With the continuous support of the National Basic Research Program of China from the Ministry of Science and Technology,a Chinese common wheat core collection(CC)and a mini core collection(MCC)were established after genotyping 5,029 candidate accessions at 78 SSR loci[48].The MCC contains 231 accessions,or 1%of the basic collection(23,135 accessions),with an estimated 70%of the total genetic variation in the CC.Accessions in the core collection,together with additional accessions,were genotyped using CAPS markers in a genome wide association study(GWAS)of yield traits[49–51].For instance,by genotyping 1520 accessions from the core collection at two sucrose synthase loci(TaSus1 and TaSus2),Hou et al.found significant differences between haplotypes that correlated with differences in thousand grain weight among 348 modern Chinese cultivars.Yield-favored haplotypes were enriched in cultivars released since the beginning of the last century in China,as well as in accessions from Europe and North America.This work indicates that the endosperm starch synthesis pathway had been a major target of selection in global wheat breeding for higher yield[49],and that further improvement could be made.

14.Enforcement of wheat functional genomics research by young investigators

The significant achievements in wheat have allured successful young scientists both domestically and overseas trained to enter the wheat functional genomics field.Excellent outcomes from young investigators have been made in transcriptomics with significant contributions on the roles of micro-RNA[23,52,53],nutrient uptake,disease resistance[54,55],and grain yield[28].We believe that increasing numbers of young investigators will join the wheat research community and will significantly lift wheat research quality and expedite the discovery of new knowledge that will further contribute to food security of the people in China and the world.

Acknowledgements

The editors express their gratitude to Professor Robert A.McIntosh,University of Sydney,as an English editor and wheat expert in assisting to make this special issue available to the readers of The Crop Journal.This work is supported partly by the National Key R&D Program for Crop Breeding of China to L.M.(No.2016YFD0101004).

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