Crop domestication, green revolution, and breeding

Steve Strauss

Source for many slides: www.plantcell.org/cgi/doi/10.1105/tpc.111.tt0511

Strauss the ~human

• Father of two (31, 34) that are grown and gone• Sporty for old fart

– Varsity and club soccer referee (>20 years)– Regular runner and occasionally mtn biker

• Avid hiker, non-technical mtn climber• Craft beer snob

Bella and wife Barb on Mt. Hood, Oregon a few years ago

Strauss research

• Web site: http://people.forestry.oregonstate.edu/steve-strauss/

• Current research– Genetic engineering (GE) – poplars and eucalyptus

• Engineer sterile trees to minimize or avoid gene flow• Industrial consortium (22 years)

– Genomic basis of hybrid vigor in trees• Focus on poplar interspecies hybrids• Non-GMO genetics and breeding

Short-rotation poplars an ag crop in Oregon

Former Director, OSU Outreach in Biotechnology Program

Available itunesU

Forty lectures, diverse aspects

The Distant PastCrop plant domestication

The Recent PastHybrid seedThe (First) Green Revolution

Now and Into The FutureBreeding, recent advances in breeding technologies Genetic engineering (next lecture)

Lecture overview

The Distant Past (>10,000 years ago to 1900)

• Homo sapiens originated 250,000 - ~1 million years ago

• Major crops were domesticated ~ ~ 5,000- 15,000 years ago

• The development of human civilizations is correlated with the development of agriculture

Karol Schauer

Pulitzer Prize winner

Agriculture enabled cities, culture, and thus advanced technologies

And then the spread of humans with their ag- and urban animal-associated diseases (to aid in conquest) moved around the globe

X

X

How did people begin to cultivate plants?

It is thought to have been a gradual change from seeking and following food sources to semi-settled migration and finally permanent settlements X

What is domestication?

• Wikipedia

• Domestication (from the Latin domesticus: "of the home") is the cultivating or taming[1] of a population of organisms in order to accentuate traits that are desirable to the cultivator or tamer.

• The desired traits may include a particular physical appearance, behavioral characteristic, individual size, litter size, hair/fur quality or color, growth rate, fecundity, lifespan, ability to use marginal grazing resources, production of certain by-products, and many others.[2]

• Domesticated organisms may become dependent on humans or human activities, since they sometimes lose their ability to survive in the wild.[3]

Plants were domesticated in parallel in several regions of the globe – “centers of origin”

Reprinted by permission from Macmillan Publishers Ltd.: [Nature] Diamond, J. (2002). Evolution, consequences and future of plant and animal domestication. Nature 418: 700-707, copyright 2002.

Wheat, barley, pea, lentil~ 13,000 years ago

Rice, soybean ~ 9000 years ago

Rice, bean ~ 8500 years ago

Corn, squash, bean, potato ~ 10,000 years ago

Genetic modification, in traditional sense, arose as a consequence of cultivation

Natural variation within population

Image courtesy of University of California Museum of Paleontology, Understanding Evolution - www.evolution.berkeley.edu

Planting seeds from “good” plants increased their representation in subsequent generations

The hard casings around many grains were eliminated

Photo by Hugh Iltis; Reprinted from Doebley, J.F., Gaut, B.S., and Smith, B.D. (2006). The Molecular Genetics of Crop Domestication. Cell 127: 1309-1321, with permission from Elsevier.

Teosinte, the wild relative of maize, has hard coverings over each grain. Humans selected against these during maize domestication.

During maize domestication cob size increased

Photo © Robert S. Peabody Museum of Archaeology, Phillips Academy, Andover, Massachusetts. All Rights Reserved.

Cobs from archeological

sites in the Valley of Tehuacan,

Mexico

7000 years ago

500 years ago

Decrease in branching and increase in seed size were also selected for

Image credit Nicolle Rager Fuller, National Science Foundation

Why single-stem vs. bushy maize plants during early domestication?

A. A rare mutation was fixed at the same time a, by chance, when kernel casings were selected against

B. They could better support increasingly large and more numerous cobs

C. They could be packed more tightly into a small area to increase yield

D. Farmers could more easily cultivate (remove weeds) between the rows

E. All of the above

Seeds that don’t break off were selected

WildShattering grain“Brittle rachis”Advantage –maximizes seed dispersal

DomesticatedNon-shattering grain

“Tough rachis”Advantage –

facilitates harvesting

From Konishi, S., Izawa, T., Lin, S.Y., Ebana, K., Fukuta, Y., Sasaki, T., and Yano, M. (2006). An SNP caused loss of seed shattering during rice domestication. Science 312: 1392-1396. Reprinted with permission from AAAS.

Wheat & barley show three key traits….

• Shattering resistance• Loss of dormancy• Synchronous flowering/maturity

Over time, domestication customized crops for specific uses

Food wheat and barley vs. barley for beer

• Non-adhering hull (naked): wheat/barley for food • Adhering hull: barley for beer

Domestication

Maize

Rice

Tomato

Lettuce

Banana

And many other types of modifications made

Radical changes in form: Diversity of crucifer crops derived from wild cabbage

Wildcabbage

Kale, 500 BC

Ornamental kaleLate 1900's

Cauliflower1400's

BroccoliItaly, 1500's

Cabbage, 100 AD

KohlrabiGermany, 100 AD

Brussel sproutsBelgium, 1700's

Radical changes in domesticated animalsAll dogs derived from the wolf by breeding

Many of our crops are products of extensive genomic rearrangements

From Dubcovsky, J. and Dvorak, J. (2007). Genome Plasticity a Key Factor in the Success of Polyploid Wheat Under Domestication. Science. 316: 1862-1866. Reprinted with permission from AAAS. Brassica figure from Adenosine

Common wheat is the result of interspecific hybridization between

three ancestorsPolyploid (multi-

genome) plants are often bigger and so

selected for propagation

The brassicas share three genomes recombined in various ways

Va Va VaVaVbVb VaVaVbVbVdVd

Barley, Einkorn vs. Emmer, Durum, and Bread Wheat

2n = 2x = 1430,000 genesBarley, Einkorn

2n = 4x = 2860,000 genesEmmer, Durum

2n = 6x = 4290,000 genesSpelt, Bread Wheat

Natural selection and domestication polyploidy

Many plant varieties derived from induced mutations

Calrose 76 semi-dwarf rice

High oleic sunflower

Over 2,000 crop varieties derived from mutagenesis have been commercialized

Rio Red grapefruit

Genetic basis of domesticationhas been well-studied

ALL types of mutations selected

• Single nucleotide polymorphisms• Insertions/deletions within genes• Complete gene deletion• Gene duplication/multiplication• Altered regulation (expression)

~ 30 of 30,000 genes altered in a major way during domestication of major crops

Genetic basis of domestication

• Bottlenecks and selective sweeps: Loss of genetic diversity due to selection for domestication traits

• Critical to maintain wild populations and seed banks of diversity

Domestication has reduced genetic diversity compared to wild plants

Are domestication genes similar to transgenes (GMO)?

A. Yes

B. No

Numerous genes changed during further breeding over millennia – soy example

• The best genes have been stacked together through selecting based on phenotypes.

4,000 years ago

From Brian Diers, University of Illinois

4,000 years ago 500 years ago

Numerous changes during breeding over millennia

4,000 years ago 500 years ago Present day

Numerous genes changed – and moving faster with new breeding methods

PA CHIAMSERAUP

FORTUNA BESAR 15 MARONG UNKNOWNPAROC

BLUE ROSEBPI 76 REXORO SUPREME

KITCHILI SAMBA

SINAWPAGH

UNKNOWNCINA LATISAIL TEXAS RSBR GEB24

PATNA BLUE BONNETPETA

DGWG CP231 SLO 17 BENONG

IR86 CP SLO 17 SIGADIS

IR95IR127

IR8 CHOW SUNG IR262

IR1103 TADUKAN VELLAIKARIR400 TSAI YUAN CHUNG

IR1006 MUDGOTETEP

IR1163 IR238 TN1IR1416 IR1641

IR1402IR22 TKM6 IR746A

IR1704O. nivara

IR1870 IR1614

IR2006 IR579 IR747 IR24/ IR661 IR1721

IR773 A BPI 121 GAM PAI

IR1915 B IR1833 GAM PAI 15 IR1561 IR1737

IR1916 IR833 IR2040

IR2146 IR 2055IR2061

IR5236 IR5338 Ultimate LandracesGAM PAI TSAI YUAN CHUNG

IR5657 DEE GEO WOO GEN BENONGCINA Unknow n

IR18348 LATISAIL CHOW SUNGTADUKAN MUDGO

IR64 KITCHILI SAMBA TETEPPA CHIAM SINAWPAGHSERAUPBESAR 15 UNKNOWN (JAPANESE)NAHNG MON S 4 O. nivara (IRGC 101508)VELLAIKAR MARONG PAROC

NAHNG MON S4

NMS 4

IR 64

original rice genome

Mutations

Recombinations Translocations

Deletions

Inversions

One of the most widely grown crops, indica rice IR64 is the product of a complex breeding program that has caused extensive genomic modification, mutation, deletion and rearrangement

Slide courtesy of Ingo Potrykus

Mutations of all kinds common during post-domestication breeding

The recent past – scientific plant breeding

Improvements in plant propagation and breeding were needed to keep up with population growth

Photo credits: Gartons Plant Breeders

Mendel and Darwin paved the way for scientific plant breeding

The development of hybrid corn led to a big increase in yields

A BB x A A x B The progeny of two genetically different parents often show enhanced growth – this effect is termed “hybrid vigor” or “heterosis”

Occurs in within-species and between species crosses to variable degrees

Inbreeding often precedes hybridization

Shull, G.H. (1909) A pure line method in corn breeding. Am. Breed. Assoc. Rep. 5, 51–59 by permission of Oxford University Press.

Hybrid corn was rapidly adopted because of its increased yields

A BB x A A x B

Percentage of total corn acreage

Even though farmers had to purchase seed every year,

increased yields more than offset increased costs

Shull, G.H. (1909) A pure line method in corn breeding. Am. Breed. Assoc. Rep. 5, 51–59 by permission of Oxford University Press; Economic Research Service / USDA

Norman Borlaug was a plant breeder, and “father of the green revolution”

Distinguished plant breeder and Nobel LaureateNorman Borlaug 1914-2009

One of the most significant accomplishments of 20th

century science was the development of high-yielding, semi-dwarf grain varieties

Why semi-dwarfism?

A. It was the first GMO crop

B. Easier to pick the seeds

C. Plant were prevented from lodging during rain/wind, especially when planted densely and fertilized/irrigated

D. Plants produced higher yields by wasting less energy on stems for height growth

E. C and D

Genetics:• Semi-dwarf genes (qualitative)• Straw strength (quantitative)• Plant architecture (quantitative)• Disease resistance (qualitative/quantitative)• Yield (quantitative)• Quality (qualitative/quantitative)• Nutrition (qualitative/quantitative)

Agronomy:• Fertilizers• Pesticides

• Qualitative traits are distinctive, and controlled by one or a few genes• Quantitative traits are usually controlled by many genes, and give continuous

phenotypes www.achievement.org

A wide variety of genetics, traits, and environment gave rise to the green revolution in wheat

Improved green-revolution plants led to dramatically increased crop yields

The introduction of disease-resistant, semi-dwarf

varieties turning countries from grain importers to grain

exporters

Source: FAO via Brian0918

Dwarf wheat was developed at CIMMYT – the International Maize and Wheat Improvement Center

Rice breeding at IRRI also brought huge yield increases

0

0.5

1

1.5

2

2.5

3

3.5

4

4.5

1961 20001980World rice yield (ton/ha) (FAO)

Photo courtesy IRRI

IR8, released in 1966, “…was to tropical rices what the Model T Ford was to automobiles.” It was

known as “miracle rice” because of its high yields.

Crop productivity has kept pace with population because of increased yields

Burney, J.A., Davis, S.J., and Lobell, D.B. (2010). Greenhouse gas mitigation by agricultural intensification. Proc. Natl. Acad. Sci. 107: 12052-12057.

Population (billions) Crop area (hectare)Crop production (gigaton)

Crop area has not increased as rapidly as crop production, because yields (food per hectare) have increased

Growing more food without using more land helps mitigate climate change and slow the loss of biodiversity

100% increase

>100% increase

~20% increase

Modern plant breeders use conventional and molecular methods for plant improvement

Photo credits Scott Bauer USDA; CIMMYT; IRRI; RCMI; Duke Institute for Genome Sciences and Policy

Example: Soybean breeding

Make crosses

Develop experimental lines

Select the best lines

• Soybean is a self pollinated/inbred crop. Bred similar to wheat, barley, dry beans, peanuts. – Self pollinated crops will produce

seed through crossing with itself.

Soybean Breeding – Start with diversity

1. Manually cross diverse types of plants to generate diversity, new combinations of genes

2. Hybrid = F1, highly heterozygous

F11 Aa

X

Not uniform and therefore undesirable unless one can clone (i.e., vegetative propagation, like grape, apple, banana, cassava, potato, eucalypts, poplars)

Soybean breeding – Transform heterozygosity into variation between inbred lines

1. Manually cross plants2. Inbreed plants several generations to

remove heterozygosity, make uniform3. Test thousands of inbred lines in field tests4. Further test in many environments to

develop potential varieties

F11 Aa

F2½ Aa

F3¼ Aa

F41/8 Aa

XXX X

Uniform Potential Variety

Soybean Varietal Evaluation

4. Evaluate potential varieties

5. Produce seed of varieties

Plant Breeding is a Long Term Effort - Soybean

Season Activity Season Activity

1 Make cross 6 Grow new experiment lines in small plots

2 Grow F1 7 Grow yield tests in two environments

3 Grow F2population

8 Grow yield tests in 5 environments

4 Grow F3population

9 Grow yield tests in 20 environments

5 Grow F4population

10 Repeat yield tests and increase seed

Example: Maize (Corn) Breeding

• Cross pollinated/hybrid crop. Bred similar to sunflowers, sorghum, canola

• Takes advantage of hybrid vigor (heterosis)

Maize (Corn) Breeding – heterosis testing

1. Make crosses among lines in program2. Develop inbred lines3. Test performance of inbred lines in hybrid

combinations4. Identify hybrid combinations with the greatest

performance5. Produce seed of hybrid combinations6. Companies sell hybrid seed not inbred

lines to growers (intellectual property protection)

Breeding is a Numbers Game

• Buy more lottery tickets, greater chance of winning

• Test more lines, better chance of selecting a winner as each potential lines has a unique combination of genes. • Use science to improve odds.

Breeders Have Increased Their Capacity to Phenotype

100,000’s of potential varieties will be evaluated annually.

Advances in genetic technologies increasingly contribute to improved plants

• Marker assisted selection (specific genes)

• Genomic selection (whole genomes)

• Recombinant DNA technology and transgenic plants

Photo credit: IRRI

Genetic Markers Are Being Used in Selection

• Phenotyping is expensive and inaccurate.• Identify the gene controlling the trait and directly

select for this.

Rag1 gene

Satt5400.0Satt4353

Rag17

Satt46315

Satt24520

Satt32325Satt22028

Genetic Markers Are Being Used in Selection

Collect leaf tissue Amplify specific genetic regions

Load DNA on a gel

Separate DNA on a gel, score and select

Currrent methodsNow entire process of marker generation and use is

automated and robotized – tens of housands to millions of markers on chromosomes routinely studied

Prior methods

A genome from many short sequences

Next-generation sequencing

From Glenn Howe, Oregon State University

Find SNP – single nucleotide polymorphism –markers by computational analysis

Single nucleotide polymorphism (SNP)

Parent 1 is heterozygous Parents 2 and 3 are homozygous

A C G T G T C G G T C T T A Maternal chrom.A C G T G T C A G T C T T A Paternal chrom.

A C G T G T C G G T C T T A Maternal chrom.A C G T G T C G G T C T T A Paternal chrom.

A C G T G T C A G T C T T A Maternal chrom.A C G T G T C A G T C T T A Paternal chrom.

Parent 1

Parent 2

Parent 3

SNPUsually 2 alleles

Many many loci

Genetic Markers Are Used on an Industrial Level in the Private Sector

Monsanto’s seed chipper

Marker DNA from automated systems.

Marker assisted selection (MAS): Statistically associate traits with specific genes, then select directly for the genes

Phenotype: physical expression of traits

Genotype: Look at a large proportion of DNA segements and/or genes in a genome

Photo credit LemnaTec; Anderson, L.K., Lai, A., Stack, S.M., Rizzon, C. and Gaut, B.S. (2006). Uneven distribution of expressed sequence tag loci on maize pachytene chromosomes. Genome Research. 16: 115-122.

Introgression of a disease resistance gene that can be identified via MAS

Elite tomato Poor tomato but disease resistant (resistance gene indicated)

We want to add a disease resistance trait to an “elite” tomato plant.

Step 1: Make a hybrid

We cross the two plants. Some of their progeny inherit the disease resistance trait, some don’t – how can we tell the difference?

Photo by Stephen Ausmus USDA

Step 2: Retain only plants with desired gene

We can use markers to look at their DNA and identify those with the resistance gene.It’s faster and easier than infecting them to see the phenotype

The hybrid has the traits but also undesirable traits

Is this an elite, disease-resistant tomato? No, half of its genes are from the poor tomato

Backcross to crop parent multiple times and select for the marker (or the new trait)

We have to repeatedly cross back to the elite tomato, using markers to identify plants with the disease resistance gene

Repeat until genome “cleaned enough” of DNA from donor parent (can be a wild, toxic species)

After several generations, elite, disease resistant tomato

Markers greatly accelerate breeding

programs

F. Nogue – INRA France

10 % of the genome of the cultivated tomato (3,000 genes) come from interspecies crosses

From www.eu-sol.net

Repetitive hybridization and introgression leave large marks on plant genomes

But, Most Economic Traits Controlled by Many Genes

• Locations of female (DS) (36 genes) and male (DA) (39) flowering date genes in maize.

Buckler et al. Science. 2009. 325:714-718.

Advances in genomics technologies facilitate breeding for complex traits – can sequence ~whole genome now and thus look at quantitative traits too

• Genome sequence data are available for hundreds of plant species

• Molecular breeding and mapping tools are developed for many species

• Genomic selection now common

Anderson, L.K., Lai, A., Stack, S.M., Rizzon, C. and Gaut, B.S. (2006). Uneven distribution of expressed sequence tag loci on maize pachytene chromosomes. Genome Research. 16: 115-122.

Phenomics now more limiting than genomics

Genotype analysis

Genome-wide methods make it possible to identify genes associated with complex traits, like yield or water use efficiency

Association analysis

Gene discovery

Summary• Early, scientific, and molecular phases of plant improvement• Domestication – emphasis on early, major genes that enable

cultivation, consumption• Green revolution – semi-dwarfism genes and other ag

technologies to improve cereal yields• Heterosis – breeding for hybrid vigor, natural intellectual

property protection• Clonal propagation: Sterile or highly outcrossing (fruit and

forest trees)• Marker-aided selection enables genes for major traits to be

tracked and introgressed rapidly – pest resistance, nutrition• Genomic selection enables rapid improvement of complex,

polygenic traits like yield, adaptation