A perspective on breeding and implementing durable powdery ...gbg2018.u-bordeaux.fr/files/gbg2018/presentation/o... · Powdery mildew is a problem everywhere Forces Driving Change:

A perspective on breeding and implementing durable

powdery mildew resistance Lance Cadle-Davidson

[email protected]

mailto:[email protected]

Overview

• Feed discussion: How do we ensure future generations can benefit from current efforts in PM resistance breeding? • Encourage: International collaboration to address this

• Share: experience of R-genes in Cornell breeding program • RUN1/REN2 and REN2/REN3

• Update: VitisGen2 genotyping methods for gene stacking

Value of PM resistance (California Raisin grape example, in $millions)

Adoption Lag (Years)

Adoption Rate 10 20 30 40

20% $124M 92 69 51

60% 372 277 206 153

100% 620 461 343 255

Economic incentive to accelerate and increase adoption

(Addresses trade-off between time and quality)

Julian Alston

Kate Fuller

Olena Sambucci

Wine Economics and Policy 3:90-107

Powdery mildew is a problem everywhere

Forces Driving Change: • Embedded vineyards • Costs of pesticides • Costs of fuel, labor • Environmental & Health concerns

• 2003 report from an EU commission:

“viticulture uses 40% of the crop protection products in the whole of agriculture.”

• Powdery mildew management is 10-20% of cultural costs in CA (Wine Economics and Policy 3:90-107)

Slide credit: Bruce Reisch

The rise of low-input grape cultivars

Vidoc, INRA

Merlot Khorus, Univ. of Udine Calardis blanc, JKI

Borsmenta, University of Pécs

More details in Bruce Reisch’s webinar at: www.VitisGen2.org/webinars

The Crystal Ball

How do we protect these genes for future generations? How do we predict the future?

…Data-driven strategies

hiveminer.com

Milgroom, Brewer, Frenkel, Cadle-Davidson, et al.

Pathogen genetics informs host genetics

Eastern U.S.: A center of diversity for Erysiphe necator

Coevolution of pathogen with many mapped PM resistance genes

A crystal ball?

Race specificity: Vitis rotundifolia example (RUN1)

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Fig. S3. Feechan et al.

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RUN1 in vinifera PM Resistant…Eureka!

RUN1 RUN1

Normal PM

The Plant Journal 76:661–674

Race specificity: Qualitative resistance from RUN1

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Musc4 (Adapted PM)

Normal PM RUN1 in vinifera

PM Resistant…Eureka!

Challenge with PM from Southeast U.S. PM Susceptible…sigh.

RUN1 RUN1

RUN1 RUN1


Vitis (2011) 50:173–175

Race specificity: Qualitative resistance from RUN1

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Southeast PM

RUN1 in vinifera PM Resistant…Eureka!

Challenge with PM from Southeast U.S. PM Susceptible…sigh.

Similarly, within 3 years of introduction, PM in New York could reproduce on RUN1 vines

RUN1 RUN1

RUN1 RUN1

Normal PM


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+ - + - + -

- - + + - -

- - - - - +

- - + - - -

RUN1

RUN1.2a

RUN1.2b

RUN2.1

RUN2.2

NY1-137 LNYM Musc4

Phytopathology 105:1104-1113

RUN1.2a, RUN1.2b, and RUN2.2: Redundant to RUN1?

10dpi growth: 10dpi conidiation:

9 9

3 3 0 0

9 9

5 3 0 0

9 9

5 3 0 0

9 9

5 5 5 5

9=a lot; 5=some; 0=none

Co

lon

y su

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s ra

te (

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Phytopathology 105:1104-1113

RUN1 and REN2 = additive effects?

Race specificity: Moderate-minor resistance QTL

Vineyard data 1991-2008 Horizon x Illinois 547-1 (V. rupestris B38 x V. cinerea B9)

LOD

REN3

REN2

Reisch, Karn, Cadle-Davidson, et al., unpublished data

Race specificity: Moderate-minor resistance QTL

Vineyard data 1991-2008 Horizon x Illinois 547-1 (V. rupestris B38 x V. cinerea B9)

LOD

REN3

REN2

Reisch, Karn, Cadle-Davidson, et al., unpublished data Molecular Breeding 37:1 Phytopathology 106:1159-1169

Date Chr LOD LOD

Threshold R2

08-25-11 NA NA NA NA



09-17-13 4 3.69 3.40 9.6

15 3.60 3.40 9.4

08-27-14 22 3.97 3.34 11.6


Vineyard data 2011-2014 ‘Horizon’ × V. cinerea B9

REN3

REN2 no longer detectable in vineyard

REN3 race-specific Confirmed in lab

For mapping, phenotype early!

REN2+

REN3+

REN2-

REN3-

REN2-

REN3+

REN2+

REN3-

REN2 and REN3 = additive effects

0-3%

3-12%

12-25%

25-50%

50-100% P

M f

olia

r co

vera

ge

Reisch, Karn, Cadle-Davidson, et al., unpublished data

Acknowledgments: Bruce Reisch, David Ramming, Craig Ledbetter, Andy Walker, Summaira Riaz, Pal Kozma, Matt Clark, Jim Luby, David Gadoury, Bob Seem, Ian Dry, Angela Feechan, Michael Milgroom, Joe Smilanick, Molly Cadle-Davidson, Marianna Kocsis, Paola Barba, Omer Frenkel, Marin Brewer, Raj Majumdar, Siraprapa Mahanil, Sara Lagerholm, Michelle Schaub, Anna Nowogrodzki, Hema Kasinathan, Mary Jean Welser, Paige Appleton, Wei Zhang, Nancy Consolie, Jackie Lillis, Erin Galarneau, Franka Gabler, Surya Sapkota, Avi Karn, and others

Locus Chr Vitis source Race-specific Reference MAS? REN1 13 vinifera Yes Hoffman et al. 2008 Yes REN2 14 cinerea Yes Cadle-Davidson et al. 2016 Yes

REN3 15 complex Yes Welter et al. 2007 Yes

REN4 18 romanetii ? Ramming et al. 2011 Yes REN6 9 piazeskii Pap et al. 2016 Yes REN7 19 piazeskii Pap et al. 2016 Yes

REN9 15 complex Yes Zendler et al. 2017 Yes

REN10 2 complex Teh et al. 2017 Yes

RUN1 12 rotundifolia Yes Feechan et al. 2013 Yes RUN2.1 18 rotundifolia Yes Ramming et al. 2012

new ? aestivalis Yes Ramming et al. 2012

new 7? rupestris Yes Barba et al. 2015

PM resistance in U.S. bunch grape breeding programs

Strong

Strong

Strong

What is AmpSeq? In pictures…for one amplicon

PCR1

PCR2

N7

S5

Pooling, cleanup, QC

NextGen Sequencing

S5 series barcodes identify the sample row

N7 series barcodes identify the sample column

N7 N7

S5 S5

R1

R2

Bc1 Bc2

Imagine this across 384 samples x hundreds of amplicons per sample

S501 S502

N7

01

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70

2

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Pool all samples and amplicons in one tube

QC and sequence

Any marker with a sequence basis can be converted to AmpSeq (eg here, simple sequence repeat, SSR)

CLUSTAL O(1.2.0) multiple sequence alignment

1 TCTGAGTCGGAATTTGGAATGTGGTTATGTTGTAGTGGTGGTAGT-----GGTAGTAGTGGTAGTAGTAGTGGTGGTGATGATGATGATGATGAT---AAG…

3 TCTGAGTCGGAATTTGGAATGTGGTTATGTTGTAGTGATGGTAGT-----GGTAGTAGTGGTAGTAGTAGTGGTGGTGATGATGATGATGATGAT---AAG…

9 TCTGAGTCGGAATTTGGAATGTGGTTATGTTGTAGTGGTGGTAGT-----GGTAGTAGTGGTAGTAGTAGTGGTGGTGGTGATGATGATGATGAT---AAG…

33 TCTGAGTCGGAATTTGGAATGTGGTTATGTTGTAGTGGTGGTAGT-----GGTAGTAGTGGTAGTAGTAGTGGTGGTGATGATGATGATGGTGAT---AAG…

314 TCTGAGTCGGAATTTGGAATGTGGTTATGTTGTAGTTGTGGTAGT-----GGTAGTAGTGGTAGTAGTAGTGGTGGTGATGATGATGATGATGAT---AAG…

2 TCTGAGTCGGAATTTGGAATGTGGTTATGTTGTAGTGGTGGTAGT-----GGTAGTAGTGGTAGTAGTAGTGGTGGTGATGATGATGATGATGATGATAAG…

5 TCTGAGTCGGAATTTGGAATGTGGTTATGTTGTAGTGATGGTAGT-----GGTAGTAGTGGTAGTAGTAGTG---GTGGTGATGATGATGATGAT---AAG…

8 TCTGAGTCGGAATTTGGAATGTGGTTATGTTGTAGTGAT-----------GGTAGTGGTAGTAGTGGTGGTGGTGATGATGATGATGATGATGAT---AAG…

10 TCTGAGTCGGAATTTGGAATGTGGTTATGTTGTAGTGGTGGTAGT-----GGTAGTAGTGGTAGTAGTAGTGGTGGTGATGATGATGATGAT[+9]--AAG…

62 TCTGAGTCGGAATTTGGAATGTGGTTATGTTGTAGTGATGGTAGT[+30]GGTAGTAGTGGTAGTAGTAGTGGTGGTGATGATGATGATGAT------AAG…

************************************ * ********* ***** ** *** ** *********** * ***

By electrophoresis, the top 5 alleles would all appear to be the same SSR allele.

Two of the SNPs shown here occur with multiple SSR allele sizes.

Excellent quality data from undetectable quantities of dirty DNA. Analysis of same DNA by SSR capillary electrophoresis was a mess.

In VitisGen1, GBS markers developed from one breeding program did not work in other breeding programs

Jonathan Fresnedo

Shanshan Yang

Side note on marker transferability

Horticulture Research 3:16002

Total bases (Mbp) N50 (kbp) V. cinerea B9 (pacbio) 702 226 V. cinerea B9 (10X) 427 374 V. x doaniana (10X) 472 1767 V. riparia 415 702 V. rupestris B38 (10X) 524 545 Chambourcin (10X) 523 538 Jaeger 70 (10X) 503 292 Concord (10x) 491 324 Norton (454/Illumina) 459 12 Sultanina (Illumina) 544 278 CabSav_v1 (pacbio) 591 2173 Flame (10X) 543 1980

Lance Cadle-Davidson

Jason Londo

Michael Campbell

Dario Cantu

Anne Fennell

Doreen Ware

A core genome to improve transferability: Reference genomes examined

wild

interspecific

vinifera

PN40024 chr9

Cheng Zou

Core genome was built by aligning each genome to PN40024

0

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• 70% of core genome overlaps with genes

Grapevine core genome

8 7 6 5 4 3 2

Genomes

2000 rhAmpSeq markers from core genome

Avi Karn

Cheng Zou

rhAmpSeq compatible with thousands of multiplexed markers

Avi Karn

Cheng Zou

y = 0.78x R² = 0.98

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Jonathan Fresnedo


Avi Karn

Cheng Zou

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Reads in each Marker


Avi Karn

Cheng Zou

-Lo

g(p

-val

ue)

Physical position (Mb)

GWAS Flower Sex using MLM(PCA+K) model

chr2_4825658

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Chromosome 2

Getting started with AmpSeq

• Make data analysis plan

• Order PCR1 primers with linkers

• Obtain DNA from samples of interest

• Decision point: • In-house: Order PCR2 barcode

primers, multiplex PCR mix, multichannel pipet or robot

• Outsource: Simply send primers and DNA to genotyping facility

ICPP Workshop Sunday, July 29, 2018: Hands-On Analysis of AmpSeq Data

Outreach: AmpSeq workshops

Avi Karn

Jonathan Fresnedo

Strongest R-genes already discovered? New alleles possibly redundant?

~16 R-gene QTL mapped in grapevine Are the strongest effect loci already known?

How many more will we find? Barley: 27 R-gene loci

Wheat: 41 R-gene loci, 60 alleles

Some QTL have additive effects

All are likely race-specific Justification for stacking = additivity and spectrum

Some are redundant Need knowledge of which combinations are useful

Plant Pathology 64: 1396–1406 Crop and Pasture Science 63:997-1006

• Inform strategies: Test combinations of RUN1, REN1, REN2, REN3/9, REN4, REN6, REN7 and REN10. • Example: RUN1, REN1, REN6, REN7 = 16

combinations

Which combinations are useful?

• Inform strategies: Test combinations of RUN1, REN1, REN2, REN3/9, REN4, REN6, REN7 and REN10. • Example: RUN1, REN1, REN6, REN7 = 16

combinations

• Crosses made for 18 of 28 pairs by Clark, Ledbetter, and Reisch

Which combinations are useful?

The lesson of the glass wall

• To learn about how the pathogen will overcome host resistance, plenty of lessons from Fungicide Resistance.

“Those who cannot remember the past are condemned to repeat it.” - George Santayana

Timeline from release to first report of Fungicide Resistance 1973 1977

1982 1985 1989 1990

1997 2003

Lessons from fungicide resistance

High risk: Strobilurins (Group 11); Ridomil products (Group 4); benzimidazoles (defunct Benlate and current Topsin-M, Group 1).

Medium-to-high risk: SDHIs (Group 7); Rovral (Group 2); ametoctradin (one component of Zampro, Group 45); Ranman (Group 21)

Medium risk: DMIs (Group 3); the APs (Group 9; Vangard, Scala, one component of Switch); Quintec (Group 13); Vivando (Group U 08)

Low-to-medium risk: Group 40 fungicides (dimethomorph, one component of Zampro); Elevate (Group 17); fludioxonil (Group 12).

Low risk: Mancozeb, captan, ziram, sulfur, copper, oils, salts


High risk: Strobilurins (Group 11); Ridomil products (Group 4); benzimidazoles (defunct Benlate and current Topsin-M, Group 1).

Medium-to-high risk: SDHIs (Group 7); Rovral (Group 2); ametoctradin (one component of Zampro, Group 45); Ranman (Group 21)

Medium risk: DMIs (Group 3); the APs (Group 9; Vangard, Scala, one component of Switch); Quintec (Group 13); Vivando (Group U 08)

Low-to-medium risk: Group 40 fungicides (dimethomorph, one component of Zampro); Elevate (Group 17); fludioxonil (Group 12).

Low risk: Mancozeb, captan, ziram, sulfur, copper, oils, salts


What can we learn from fungicide strategies?

Be honest: the pathogen will win battles; our job is to delay or prevent it from winning the war.

For fungicides

Combine different modes of action

• Often a higher risk with lower risk

Rotate to effective, unrelated chemicals

Limit size of pathogen population

• Don’t use at-risk to rescue

Limit reproduction of resistant individuals

For quantitative resistance, increase dose or activity

Apply best chemicals when disease control is most important.

For host resistance

Combine different mechanisms

• But all are high risk

Cannot rotate

Keep nearby vines disease-free

• Don’t use at-risk to rescue

Limit reproduction of virulent

Cannot increase dose after planted

Apply chemicals after flowering, before pathogen’s sexual phase? Engage pathologists!

Lessons from Wayne Wilcox

• Barley PM: Resistance typically lasts 3 years for individual genes, 5 years for stacked genes. • Exception: mlo effective since 1940s.

• Oat rust (left): Virulence within 1-2 years.

• Quantitative resistance (QR) typically involves at least 4-5 QTL and may be more durable than qualitative resistance (but also exceptions).

• Gene pyramids: redundancy, additive effects, or synergistic mechanisms? • HR + reduce sporulation or ontogenic resistance • Need more info

• Variety mixtures

What can we learn from other crops?

Infect Genet Evol. 2014:446–455

Mol Ecol. 10:1–16

Annu Rev Phytopathol. 14:355–382

Oat rust

• Education: Growers are familiar with fungicide stewardship Develop best practices for managing genetics (built into vine) and chemistry (applied by

grower).

• Patented variety, not otherwise managed • Adding cultural practice requirement is possible, but mechanism usually not exercised.

• Managed varieties (eg SweeTango apple): dictate who and how club varieties are grown • Contractually require growers to conduct certain cultural practices • Lease the vines, with contractual obligations

Legal/educational assets to protect R-genes

Human nature: Ensuring that growers cooperate (apply the requested pesticides, timing, and rates) could be challenging.

Thank you to Peter Cousins, Matt Clark, Bruce Reisch, and Craig Ledbetter for helpful comments!

Limited supply of useful, non-redundant resistance alleles available->need durability.

• Stacking with knowledge of complementarity should be helpful. • Minor resistance effects of genetic background should help as well.

• Annual fungicide application(s) will be critical. • Remove ‘No-spray’ from lexicon. • (Biologicals are a viable option.) • Use education to encourage Annual spray(s). • Manage varieties to mandate Annual spray(s) contractually. • Spray when fruit is susceptible; other sprays will depend on local epidemiology

• Powdery mildew management in nearby blocks will be critical.

• Variety mixtures (different R-gene stacks in adjacent rows) may be helpful.

At Cornell/USDA:

• We can receive other R-genes for standardized phenotyping.

• Need an effort like OsCaR in center of origin, as a crystal ball of best management practices.

My recommendation from this

VitisGen2 Genotyping and PM Goal

Provide germplasm, strategies, protocols, and marker technology (cost-effective and accessible) to make PM resistance breeding easy, efficient, and effective.

VitisGen2 Genotyping and PM Goal

Provide germplasm, strategies, protocols, and marker technology (cost-effective and accessible) to make PM resistance breeding easy, efficient, and effective, and integrated strategies for durability and increased adoption.

Strategies to increase adoption

Acknowledgments

Breeding Team: Bruce Reisch, Lead Lance Cadle-Davidson Matt Clark Anne Fennell Harlene Hatterman-Valenti Chin-Feng Hwang Craig Ledbetter Jason Londo Rachel Naegele Andy Walker

Funding: USDA-NIFA Specialty Crops Research Initiative

Project Number 2017-51181-26829

Genetics Team: Jason Londo, Lead Lance Cadle-Davidson Dario Cantu Qi Sun Peter Schweitzer Anne Fennell

Powdery Mildew Team: Lance Cadle-Davidson, Lead David Gadoury Mark Rea

Executive Committee: Bruce Reisch, Lead Lance Cadle-Davidson Jason Londo Gavin Sacks Tim Martinson Julian Alston

Trait Economics Team: Julian Alston, Lead Olena Sambucci Karina Gallardo Bradley Rickard

Extension and Outreach Team: Tim Martinson, Lead Matthew Clark Michelle Moyer Keith Striegler

Fruit Quality Team: Gavin Sacks, Lead Anna-Katharine Mansfield Rachel Naegele, TG Lead

Project Manager: Fred Gouker

Helpful discussions Peter Cousins, Ian Dry, Ed Buckler

Documents

A perspective on breeding and implementing durable powdery ...gbg2018.u-bordeaux.fr/files/gbg2018/presentation/o... · Powdery mildew is a problem everywhere Forces Driving Change: