To redefine plant breeding with genomics

Sanwen Huanghuangsanwen@caas.net.cn

KLV125, November 10, 2011

Chinese Academy of Agricultural SciencesBeijing, 100081, China

Two solutions to feed China

1) Better seeds2) Farm cooperative

Plant breeding contributed

>50% of growth in agricultural production.

First generation plant breeding

Rice

SoybeanWheat BarleySunflower

Maize

Potato

Sorghum

~10,000 years ago

Darwin 1859 Mendel 1865 Morgan 1911

Second generation plant breeding

Borlaug 1950s Yuan Longping 1960s

P E R S P E C T I V E S

Hybrid maize. Within ten years of Jones’proclamation, the first breeders were produc-ing successful hybrids. Beginning in the early1930s, interest in, and demand for, hybridmaize rose steadily among farmers in theUnited States16 (FIG. 2a).Maize breeders havecontinually turned out higher-yieldinghybrids, year after year17–19 (FIG. 2b), and farm-ers have adopted them after cautious trials ontheir own farms. In 1997,United States maizeyields averaged 8 tons hectare–1, comparedwith 1 ton hectare–1 in 1930 (REF. 20).

Hybrids were not entirely responsible foradvances in maize yields, however. Startingaround the 1950s, the increasingly widespreaduse of synthetic nitrogen fertilizers, chemicalweed killers, and more efficient planting andharvesting machinery also contributed tohigher yields17–19,21.

Surprisingly, improvements in heterosishave not contributed to higher yields.Experiments have shown that heterosis(calculated as the difference in yieldbetween a single cross hybrid and the meanof its two inbred parents) is unchangedover the years. The yields of the inbred lineshave risen at almost the same rate as hybridyields22. It seems that yield gains have comeprimarily from genetic improvements intolerance to stresses of all kinds (such astolerance to disease and insects, denseplanting, drought or low soil fertility). Thenewer hybrids are tougher than their predecessors and shrug off droughts (forexample) that would have damaged the older hybrids and devastated their open-pollinated parents.

but, to this day, there is no completely satis-factory explanation for the phenomenon ofheterosis in maize or in any other species14.Fortunately, a lack of understanding hasnever hindered the use of the phenomenon.

But in the 1920s, these problems were allin the future. The ‘hybrid maize’ enthusiastswere occupied primarily with findinginbreds that made outstanding hybrids. Aswith many interest groups, the ‘hybridmaize breeders’ came to know each otherand developed an informal exchange ofinformation and materials. They neededeach other’s inbreds, for no one had enoughof them to make a series of good double-cross hybrids.

In the 1920s (and for some decadesthereafter), the primary source of ideas, the-ories and germ plasm was the public-sectormaize breeders at the agricultural collegesand in the USDA. They published their find-ings in the scientific literature and, impor-tantly, furnished breeding materials, such asinbred lines, to all that asked. The public sec-tor through the extension services (depart-ments through which farmers’ and scientistsexchange information) of its agriculturalcolleges, also effectively educated the farm-ing community (and the interested non-farming public) about the advantages ofhybrid maize.

Without the contributions from the public sector, the commercial maize breed-ers probably could not have succeeded in the early years, for individually they simplydid not have enough inbred lines orenough knowledge about how best to makeand test hybrids15.

NATURE REVIEWS | GENETICS VOLUME 2 | JANUARY 2001 | 7 1

Figure 1 | Detasselling maize plants Detasselling — pulling tassels — is vital for the production ofhybrid maize. The detasselled plants are called ‘females’; they will bear the hybrid seed. In the earlyyears, men on foot did the detasselling, as in this photo from the 1930s. In later years, high schoolboys and girls were recruited to do the job, also on foot. Today, youths are still the chief laboursource, but they usually ride in special motorized carriers, thereby increasing the speed andprecision of their work. (Image courtesy of Pioneer Hi-Bred International, Inc.)

01930 1935 1940 1945

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Figure 2 | Maize hybrids: area planted andyield potentials. a | Per cent of maize areaplanted to hybrids, from 1930 to 1960, in Iowa(red) and in the United States (green). During the1930s, hybrids almost completely replaced open-pollinated varieties in most of the Corn Belt and,by 1960, virtually all maize plantings in the UnitedStates were hybrid. Yield gains paralleledincreases in area planted to hybrids. Iowa maizeyields advanced on average from 2 tons hectare–1

in 1930 to 5 tons hectare–1 in 1960; United Statesmaize yields advanced from 1 ton hectare–1 in1930 to 4 tons hectare–1 in 1960. (Adapted fromREF. 20.) b | Grain yields (in tons hectare–1) of 36popular hybrids introduced in central Iowa from1934 to 1991, according to tests conducted incentral Iowa in 1991–1994. New maize hybridsyield more than their predecessors, and are alsocontinually being improved for other traits, suchas disease resistance and tolerance to drought.Researchers have concluded that, on average,improvements in hybrids have been responsiblefor about 50–70% of the on-farm yield gains sincetheir introduction, and changes in agronomicpractices (such as more fertilizer and better weedcontrol) have been responsible for the remainder.(Adapted from REF. 18.)

© 2001 Macmillan Magazines Ltd

Pioneer 1930s

72 | JANUARY 2001 | VOLUME 2 www.nature.com/reviews/genetics

P E R S P E C T I V E S

tus as independent seed savers, and eventhough hybrids as such were looked on asstrange new creations of science. Havingtraced the development of hybrid maize, theseand related questions can be addressed.

Farmers gave up their status as indepen-dent seed savers because they found by expe-rience that they would profit more by doingso. They were already giving up their status asindependent power suppliers on their farms,for example, as they moved from horse powerto tractor power and from hand harvest tomechanical maize pickers.

Although farmers viewed hybrids as newand strange creations of science, they saw noadverse effects on either their crops or theirlivestock. It is true that, in the early days,some farmers feared that the abnormallyhigh yields from hybrids would drain the soilof needed fertilizer elements. And there werecomplaints about some of the first hybrids,to the effect that the kernels were too flintyand hard for cows to chew. Seed companiesbred new hybrids to satisfy the second com-plaint, and the first concern turned out to bewithout foundation if normal soil fertilitypractices were used.

The farmers’primary fear was not that sci-ence might create unmanageable ‘monsters’(today’s widespread point of view), but thatscientists claimed more power to help agricul-ture than they really possessed.

Public and private breeders. In the early yearsof the hybrid era, people were undecidedabout how to deliver hybrids to the farmer.Farmers had the option to produce them ontheir own farm using single cross parent seedpurchased from the agricultural colleges,or topurchase ‘ready to plant’ hybrid seed fromfarmer cooperatives or from commercial seedcompanies (FIG. 3). All methods were tried,butin the end the seed companies turned out tobe the farmers’ choice.

Once the advantages of hybrids (and thefact that farmers would buy them) were shown,seed companies sprang up across the country,especially in the Corn Belt states15 (FIG. 4).Starting with four pioneering companies, thenumbers grew exponentially in the 1930s. By1995, 305 independent companies wereinvolved with the production and sale of hybridmaize seed. As with most industries, a smallnumber of large companies dominated thebusiness, accounting for perhaps 70% of thesales.Despite their small market share, the smallcompanies have an important role in the indus-try.They provide an alternative to farmers whodo not want to buy from the larger companies.

The exchange of information and breed-ing materials among private- and public-sec-tor breeders changed as the seed industrymatured. Almost from the beginning, seedcompanies kept the pedigrees of their hybridssecret and they soon stopped trading theirinbred lines. By about the mid-1930s, allexchange of inbreds and other advancedbreeding materials was one-way, from thepublic to the private sector.

The roles of the public- and private-sectorbreeders also changed. The large companieswith strong breeding programmes hadincreasingly less need for inbreds developed bythe public sector, although the smaller compa-nies still depended on them.Over time,‘foun-dation seed companies’ were formed expresslyto breed inbred lines for lease to the small seedcompanies, thereby filling the role of the pub-lic-sector breeders. The public-sector breedersin turn shifted their primary emphasis fromthe development of inbreds and hybrids tostudying the theoretical basis for producingimproved inbreds and hybrids, as well as otherneeded aspects of maize-breeding research.

The relationship between public and pri-vate sector breeders still remains close; theyhave mutually supportive roles in the nation’smaize breeding programme.

Consequences of hybrid maizeAcceptance. In the opening paragraphs of thisarticle I asked why the maize hybrids wereaccepted without public outcry in the 1930s,even though farmers had to give up their sta-

An important change in hybrid seedproduction and performance was, in asense, a byproduct of the increases ininbred yield. By the 1960s, the newestinbreds were so high-yielding that itbecame practical to use them as seed par-ents, and so to produce single cross hybridsfor sale. The best single crosses alwaysyielded more than the best double crossesbut, as noted earlier, commercial produc-tion of single cross hybrids was not feasiblein the first decades of hybrid maize breed-ing because of the low yield potential ofinbreds from that era.

Figure 3 | The introduction of hybrid maizeseeds. The ‘seed corn companies’ effectively andenergetically introduced hybrid maize to cautiousfarmers. They recruited well-known andrespected farmers as part-time salesmen,working on commission. They gave smallamounts of free seed of new hybrids to farmersand encouraged the prospective customers tocompare them with their present varieties on theirown farms and using their own farming methods.The salesman and/or his supervisor often wouldhelp the farmer harvest the comparison. In theprocess, the sales people learned about thefarmers’ needs and desires in maize hybrids,which they passed on to the breeders. So, therelationship between farmers and seedcompanies from the beginning was almost on aneighbour to neighbour basis. The relationshipremains much the same today, with modificationsbecause of the changing nature of farming andfarmers (much larger scale, more advancedtechnologically and more business-like). Image courtesy of Pioneer Hi-Bred International, Inc.

Figure 4 | Maize quality control in the earlyyears. The fledgling seed companies devised a‘sorting belt’, allowing inspectors to examineevery ear before shelling. They wanted to be surethe seed ears were free of damage from diseaseor insects, and of the right type. Women replacedmen in many of the seed production operationsduring the Second World War, when young menwere in the armed services. Image courtesy of Pioneer Hi-Bred International, Inc.

© 2001 Macmillan Magazines Ltd

Second generation plant breeding

Plant Breeding

the art and science of changing the genetics of plants for the benefit of humankind.

Watson and Crick, 1953 Human Genome, 2001 Rice genome, 2002

Third generation plant breeding

New tech

600Gb per run

0"

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1999" 2000" 2001" 2002" 2003" 2004" 2005" 2006"

Gb"Produc4on"by"year"

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Gb"

Gb"Produc5on"by"year"

to 100,000 in 2010

100,000 Gb2010Sequence in

database

~100,000X!

$0.1 $0.20/Mb!

$20,000/Mb!

Cost of Sequencing ($ per million bases) !

Moore’s Law!

Sequencing!

Sequencing goes faster than the Moore’s law

What does this mean to plant breeding?

We can transform plant breeding from craftsmanship to informatics. It is like to turn on light in a dark room.

The Cucumber Genome

ED ITOR IAL

NATURE GENETICS | VOLUME 41 | NUMBER 12 | DECEMBER 2009 1259

Cool as a cucumberThe genome of the seventh plant to be sequenced, Cucumis sativus L., was assembled using the conventional long-read Sanger sequencing and higher-throughput short-read technology. This genome is the entry point for exploring the diversity and function of the Cucurbitaceae family of agriculturally important plants. Its compact genome, without evidence of recent duplication, will be useful in comparative analysis of plant genome evolution.

Again and again Charles Darwin found inspiration in the cucumber and its fellow cucurbits.

The first trait to strike him was the unplantlike motility of the vine’s tendrils, organs adapted to the habits of climbing and running. Use resulted in adaptation, disuse in diversification and loss.

In the varieties which grow upright or do not run and climb, the tendrils, though useless, are either present or are represented by various semi-monstrous organs, or are quite absent.

Then he noted the diversification of marrow, gourd and melon fruit forms under agricultural selection and pondered the irreducible essence of species identity. He decided to trust the biological species concept, namely that different species cannot produce fertile offspring.

If we were to trust to external differences alone, and give up the test of sterility, a multitude of species would have to be formed out of the varieties of these three species of Cucurbita.

Having a biological definition of species identity, Darwin was then able to unravel the relationship between species and apparently stable, taxonomically important traits without fear of arguing in a circle. He contrasted these traits with variable features found within a species. He was also able to identify convergent evolution under selection of the fruit morpholo-gies of distinct species of melons and cucumbers (C.R. Darwin, The Variation of Animals and Plants under Domestication 1st edn., 2nd issue, vol. 1, John Murray, London, 1868).

Now, on p 1275, Sanwen Huang et al. report the de novo assembly and annotation of the 243.5-Mb genome of the “Chinese long 9930” inbred line of cucumber and the use of a linkage map in the assembly process to tie the assembled contigs to the chromosomes. The Illumina GA technology has proven practical, so now many diverse lines can be rapidly sequenced to enable marker-assisted breeding of high-yield-ing, disease-resistant, and fresh green-scented cucumbers, along with melons, squash and pumpkins.

Cucumber and melon diverged 4–7 million years ago, and C. sativus carries chromosome fusions that distinguish the cucumber karyotypes from those of melon (C. melo) and a more distant relative, the watermelon (Citrullus lanatus). Were he here today, Darwin could see that these sets of chromosomes physically reinforce the biological species barrier to fertility, were the (widely varying) sexual systems of the plants to per-mit crossing.

What would Charles do next, equipped with genomes? No doubt he would be most intrigued to compare the genesis of the woody and non-woody tendrils of grapevine and cucum-ber, respectively. Then he might scan for signatures of plant-human coadaptation during the domestication processes of early agricultural humans. Then he might travel to investi-gate the adaptations contributing to the success of Cucumis dipsaceus, the wild spiny cucumber originating in Eastern Africa that is now invading the Galapagos Islands he once explored.

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中国农业科学院蔬菜花卉研究所 Institute of Vegetables and FlowersChinese Academy of Agricultural Sciences

Bernard de Geus

The Potato Genome

OUTLOOKAlzheimer’s

disease

NATURE.COM/NATURE14 July 2011 £10

Vol. 475, No. 7355

HISTORY

PURE JOY

Arcane mathematics that changed the world

PAGE !66

EVOLUTION

GIANT DINOSAURS

Seeds of greatness in small sauropod ancestors

PAGE !59

NEUROSCIENCE

SPINAL CORD REGENERATION

Restoring breath control after neck injury

PAGES !78 & !96

THE POTATO GENOME

sauropod ancestorsPAGE !59

The DNA sequence of the South American tuber eaten around the world PAGE !89

T H E I N T E R N AT I O N A L W E E K LY J O U R N A L O F S C I E N C E

Cover 14 July.indd 1 08/07/2011 17:39

ARTICLEdoi:10.1038/nature10158

Genome sequence and analysis of thetuber crop potatoThe Potato Genome Sequencing Consortium*

Potato (Solanum tuberosum L.) is theworld’smost important non-grain food crop and is central to global food security. Itis clonally propagated, highly heterozygous, autotetraploid, and suffers acute inbreeding depression. Here we use ahomozygous doubled-monoploid potato clone to sequence and assemble 86%of the 844-megabase genome.We predict39,031 protein-coding genes and present evidence for at least two genome duplication events indicative of apalaeopolyploid origin. As the first genome sequence of an asterid, the potato genome reveals 2,642 genes specific tothis large angiosperm clade. We also sequenced a heterozygous diploid clone and show that gene presence/absencevariants and other potentially deleterious mutations occur frequently and are a likely cause of inbreeding depression.Gene family expansion, tissue-specific expression and recruitment of genes to new pathways contributed to theevolution of tuber development. The potato genome sequence provides a platform for genetic improvement of thisvital crop.

Potato (Solanum tuberosum L.) is a member of the Solanaceae, aneconomically important family that includes tomato, pepper, aubergine(eggplant), petunia and tobacco. Potato belongs to the asterid clade ofeudicot plants that represents ,25% of flowering plant species andfromwhich a complete genome sequence has not yet, to our knowledge,been published. Potato occupies a wide eco-geographical range1 and isunique among themajorworld food crops inproducing stolons (under-ground stems) that under suitable environmental conditions swell toform tubers. Itsworldwide importance, especiallywithin thedevelopingworld, is growing rapidly, with production in 2009 reaching 330milliontons (http://www.fao.org). The tubers are a globally important dietarysource of starch, protein, antioxidants and vitamins2, serving the plantas botha storage organ anda vegetative propagation system.Despite theimportance of tubers, the evolutionary and developmentalmechanismsof their initiation and growth remain elusive.Outside of its natural range in South America, the cultivated potato

is considered to have a narrow genetic base resulting originally fromlimited germplasm introductions to Europe. Most potato cultivars areautotetraploid (2n5 4x5 48), highly heterozygous, suffer acuteinbreeding depression, and are susceptible to many devastating pestsand pathogens, as exemplified by the Irish potato famine in the mid-nineteenth century. Together, these attributes present a significantbarrier to potato improvement using classical breeding approaches.A challenge to the scientific community is to obtain a genomesequence that will ultimately facilitate advances in breeding.To overcome the key issue of heterozygosity and allow us to gen-

erate a high-quality draft potato genome sequence, we used a uniquehomozygous form of potato called a doubled monoploid, derivedusing classical tissue culture techniques3. The draft genome sequencefrom this genotype, S. tuberosum group Phureja DM1-3 516 R44(hereafter referred to as DM), was used to integrate sequence datafrom a heterozygous diploid breeding line, S. tuberosum groupTuberosum RH89-039-16 (hereafter referred to as RH). These twogenotypes represent a sample of potato genomic diversity; DM withits fingerling (elongated) tubers was derived from a primitive SouthAmerican cultivar whereas RH more closely resembles commerciallycultivated tetraploid potato. The combined data resources, allied to

deep transcriptome sequence from both genotypes, allowed us toexplore potato genome structure and organization, as well as keyaspects of the biology and evolution of this important crop.

Genome assembly and annotationWe sequenced the nuclear and organellar genomes of DM using awhole-genome shotgun sequencing (WGS) approach. We generated96.6 Gb of raw sequence from two next-generation sequencing (NGS)platforms, Illumina Genome Analyser and Roche Pyrosequencing, aswell as conventional Sanger sequencing technologies. The genomewas assembled using SOAPdenovo4, resulting in a final assembly of727Mb, of which 93.9% is non-gapped sequence. Ninety per cent ofthe assembly falls into 443 superscaffolds larger than 349 kb. The 17-nucleotide depth distribution (Supplementary Fig. 1) suggests a gen-ome size of 844Mb, consistent with estimates from flow cytometry5.Our assembly of 727Mb is 117Mb less than the estimated genomesize. Analysis of theDMscaffolds indicates 62.2% repetitive content inthe assembled section of the DM genome, less than the 74.8% esti-mated from bacterial artificial chromosome (BAC) and fosmid endsequences (Supplementary Table 1), indicating thatmuch of the unas-sembled genome is composed of repetitive sequences.We assessed the quality of theWGS assembly through alignment to

Sanger-derived phase 2 BAC sequences. In an alignment length of,1Mb (99.4% coverage), no gross assembly errors were detected(Supplementary Table 2 and Supplementary Fig. 2). Alignment offosmid and BAC paired-end sequences to theWGS scaffolds revealedlimited (#0.12%) potential misassemblies (Supplementary Table 3).Extensive coverage of the potato genome in this assembly was con-firmed using available expressed sequence tag (EST) data; 97.1% of181,558 available Sanger-sequenced S. tuberosum ESTs (.200 bp)were detected. Repetitive sequences account for at least 62.2% of theassembled genome (452.5Mb) (Supplementary Table 1) with longterminal repeat retrotransposons comprising the majority of thetransposable element classes, representing 29.4% of the genome. Inaddition, subtelomeric repeats were identified at or near chromo-somal ends (Fig. 1). Using a newly constructed genetic map basedon 2,603 polymorphic markers in conjunction with other available

*Lists of authors and their affiliations appear at the end of the paper.

0 0 M O N T H 2 0 1 1 | V O L 0 0 0 | N A T U R E | 1

Potato Genome Sequencing Consortium14 countries and 28 institution

High-profile visit from Wageningen, 2005

2005年工作总结• 艾菲特·雅可布森（Evert Jacobsen）教授荣获2005年度中国国际科技合作奖，由温家宝总理在全国科技大会宣布。

中国驻荷兰大使薛捍勤女士向雅可布森夫妇表示祝贺！

Prof. Evert Jacobsen got his big award, 2006

1）Dicot evolution

Rosids

Asterids25% flower plants

Asterid-specific genes: 2,642Potato-specific: 3,372

2) Genomic basis of inbreeding depression

Potato suffers acute inbreeding depression that likely involve thousand genes

DM: 1XRH: 2X

3) Tuber biology

Supplementary Figure 9. Proposed roles of FT homologues in potato. A, Simplified Arabidopsis pathway, redrawn according to Michaels (ref. 57 in Supplemental Text). B, Proposed potato pathway. SP3D regulates flowering time, SP6A regulates tuber initiation and SP5G represses sprouting. A functional homolog of FD-L exists in potato (S. Prat, personal communication).

A. Simplified Arabidopsis pathway

B. Proposed potato pathway

WWW.NATURE.COM/NATURE | 22Genes for tuber biotic resistance and tuber initiation and sprouting

Prat et al., Nature 2011

“The breakthrough holds out the promise of boosting harvests of one of the world's most important staple crops.”

“...this is a first big step for scientists as well as political leaders anxiously watching the vagaries in the world's food supply.”

Press coverage

Traditional potato breeding10－12 years

1,000,000

100,000

40,000

4,000

1,000 250

40

20

4

1

Genomics-based breeding4-6 years

12 trait genes/cross

1,000,000

250

20

1

• sow seeds in vitro• type trait genes•multiply candidadate

0.5 year

• field observation•more disease test•more quality analysis

1.5 year

• yield stableness test•multiply seed potato2－4 year

“One potato genome unravelled, three to go!”

Tetraploid genome sequencing remains a huge challenge

Ally for true potato seedsto create a potato propagated and bred in a tomato way

A new paradigm in potato breedingPim Lindhout

EAPR meeting, OULU, FinlandJuly 25th, 2011

www.solynta.com

EAPR meeting, OULU, Finland

novomeinnovative agriculture

Mr. Geert Veenhuizen, may you rest in peace!

100+ plant species: from algae to angiosperm, including 60 major crops, evolutionary continuum of each gene family.

100+ genotypes/species: core collections, major version of genetic variation

100 x 100 Plant Genome Project

Tree of plant kingdom

95%Arable land

Paradigm shift for plant biology

Major ag-biological questions

1. C4 photosynthesis2. N2 fixation3. Seed and flower development4. Heterosis

C4

1. C4 photosynthesis

C3

2. N2 fixation

withProf. Ton Bisseling

Understanding symbiosis by evolutionary genomics!

3. Seed and flower

development

Out of the past.

Tiny Amborella sits

at the bottom of the

angiosperm family tree.

Seed

Flower

4. Heterosis

Now: 7B2050: 9B

To the expanding world’s population requires innovation!

Redefine Plant Breeding

NEW: the science and technology of optimizing the genome of plants for the benefit of humankind

OLD: the art and science of changing the genetics of plants for the benefit of humankind.

Rice 3.0High partition in seeds

N2 fixation+droughttolerance

C4photo-

synthesis

Strongheterosis

Durable resistance, less pesticide

“The people who are crazy enough to think they can change the world, are the ones who do. ”

The education centre of the third generation of plant breeders