Dissecting the genetic architecture of salinity tolerance

in the wild tomato Solanum pimpinellifolium

PhD Proposal Defense
Mitchell Morton
14th December 2017
Committee members:
Prof. Mark Tester (chair), Prof. Vladimir Bajic, Prof. Simon Krattinger
© Linda Polik
Growing pains – the increasing demands of a rising population

Population projected to rise to ~10 billion by 2050.

a
Two of the greatest challenges will be meeting increased demand for:

FOOD ⬆50% FRESHWATER ⬆55%

Tester & Langridge (2010) Science 327: 818-22 Marchal et al. (2011). OECD environmental outlook to 2050
Prognostics

“” The consensus view is that current systems are likely capable of

producing enough food, but to do so in an inclusive and sustainable
manner will require major transformations.
FAO, 2017
“”
Global Hunger Index 2016

…Hunger is likely to persist regionally.

• 800 million undernourished

• 2 billion suffer micronutrient deficiencies

Mostly in Sub-Saharan Africa and South Asia

http://www.globalhungerindex.org/
Closing the yield gap

Adapted from FAO (2017)

Adapted from Mueller et al., 2012

#1 Irrigation limitation – water scarcity

Mekonnen & Hoekstra (2016). Science advances, 2(2) National Geographic, March 2010
Water scarcity – the fault of salt?

Salinity stress is a major constraint to plant performance

 ~$30 billion in agricultural losses annually

Salinity affects:
6% of cultivated area
20% of irrigate area

 Salt tolerant crops would help combat water scarcity and losses from
salinity stress and thus food insecurity.
Salinity stress in plants

Salinity stress
• Osmotic component
Increased osmotic potential in soil
• Ionic component
Toxic accumulation of Na+ in aerial tissues

w th
gro
al se
r m ha
No i cp
ot
se
Growth rate

m
Os h a
cp
ni
Io Osmotic
& Water
potential
Na+ Na+
Time
Salinity tolerance in plants

Salinity tolerance mechanisms

• Osmotic: Control the flow of water
Signalling; Osmotic regulation (compatible solutes, Na +…)
• Ionic: Control the flow of Na+
PM Channels and transporters
• Tissue: Control the effect of Na+
Compartmentalisation; Compatible solutes
• Also developmental adaptations…

 Salinity tolerance is a complex, subjective trait

Na+ Na+
Improving salinity tolerance – Challenges

• Complexity of salinity tolerance

 Comprehensive phenotyping
• Limited genetic resources in domesticated varieties
 Wild genetic resources

Tanksley & McCouch (1997)

The wild tomato Solanum pimpinellifolium – a genetic treasure chest

• Close wild relative of cultivated tomato

Diversity panel
 important, nutritious crop worth $160b annually ~ 300 S. pimpinellifolium accessions
• Stress-tolerant Colom b ia

Ec ua d or

e.g. salinity, pathogens, drought, heat…

• Extensive germplasm resources (TGRC, U.C. Davis) Ga la p a g os Isla nd s
Pe ru

• Small draft-sequenced diploid genome (~700Mb)

= Sa m p ling loc a tions

Project Objective
Find QTL/genes that contribute to salinity
tolerance in a S. pimpinellifolium diversity panel using
comprehensive phenotyping and GWAS
Project outline
PHENOTYPICS GENOMICS/GENETIC
Chapter 2 Chapter 3
S
Mature plants Reference
(field conditions) genome

Chapter 5
Chapter 1 Chapter 4

Young plants Genotyping &

(controlled GWAS & Genetic analyses
conditions) Candidate analysis

ASSOCIATION
Chapter 1
Phenotyping the diversity panel
Young plants, controlled conditions (TPA)
Special Acknowledgements

TPA Team: Bettina Berger, Lidia Mischis, Nicky Bond, Fiona Groskreutz, Guntur
Tanjung, Evi Guidolin, Robin Hosking, George Sainsbury, Trevor Garnett, Helli
Meinecke, Richard Norrish

Helena Oakey
The Plant Accelerator (TPA) – System overview

High-throughput phenotyping using daily

imaging of young plants

Daily data
 RGB imaging
Projected Shoot Area, growth rates, architecture
 ∆M
Transpiration

Terminal data Experimental Design

 Shoot fresh & dry mass • 1152 carts
 Na & K content • 220 accessions
 Shoot Leaf Area • Unequally replicated
• Split-plot design
• Evaporation carts
TPA – Experimental outline
• Fill pots to weight with moist cocopeat
Potting • Determine target weight for watering

• Pretreat seeds in 50% bleach for 25min

Seed treatment & Sowing • Sow 4 seeds/pot
• Thin down to 1 seedling per pot
Thinning • Load pots into positions on conveyor belts
• Scan into the system
• Add drip tray and rubber mats
Loading
• Begin automated imaging, weighing, watering
• Salt stress at ~leaf 6 emergence
Imaging begins • Apply 200mL of 600mM NaCl to tray (rainwater for
controls)
• Salt concentration at target weight = 200mM
Salt stress • Mark youngest emerging leaf
• Harvest 14 days after salt stress
• Measure whole shoot fresh mass, dry mass
Harvest
• Collect marked leaves  Flame photometer
TPA – Description of phenotypic traits

Projected shoot area: 𝑷𝑺𝑨=Σ𝑔𝑟𝑒𝑒𝑛 𝑝𝑖𝑥𝑒𝑙𝑠 ( 𝑆𝑉 1, 𝑆𝑉 2, 𝑇𝑉 )

 
~ size, in kpixels

Absolute growth rate:

  ∆ 𝑃𝑆𝐴
𝑨𝑮𝑹=
~ kpixels gained on day t ∆𝑡

𝑹𝑮𝑹=¿ ¿
 
Relative growth rate:
~ AGR relative to total size on day t

Transpiration rate:   ∆𝑀
𝐓𝐑=
~ water (mL) transpired in on day t ∆𝑡
TPA – Terminal data shows impact of salinity stress, and natural variation

SFM: shoot fresh mass SDM: shoot dry mass

TPA – Direct biomass measurements correlate strongly with PSA

y=0.0458x − 0.636, r2=0.931 ●

y=0.0039x + 0.175, r2=0.922 ●
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Terminal PSA (kpixels)

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25 50 75 100 2.5 5.0 7.5

SFM (g) SDM (g)
TPA – Longitudinal data: smoothing, intervals and spatial corrections

Longitudinal data was:

CONTROL

250
SALT

2000

200
1500

AGR (kpixles/day)
• Modelled using cubic

PSA (kpixels)

150
1000
smoothing splines

100
500

50
• Divided into representative

0
−2 −1 0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 −2 −1 0 1 2 3 4 5 6 7 8 9 10 11 12 13 14

Days after salt Days after salt

intervals
> Int 1: Day 0 – 5

300
Int 1 Int 2 Int 3
> Int 2: Day 6 – 9

250
0.4
> Int 3: Day 10 – 14

200
0.3

TR (mL/day)

150
RGR

• Spatially corrected

100
0.2

50
0.1

0
−2 −1 0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 −2 −1 0 1 2 3 4 5 6 7 8 9 10 11 12 13 14

Days after salt Days after salt

TPA – Longitudinal data shows impact of salinity stress

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Treatment ●

●
CONTROL ●
●
2000 ●
SALT ●
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200 ●

AGR (kpixels/day)
●
1500
PSA (kpixels)

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Days after salt Days after salt

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RGR

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−2 −1 0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 −2 −1 0 1 2 3 4 5 6 7 8 9 10 11 12 13 14
Days after salt Days after salt
TPA – Interval data shows impact of salinity stress

200 ● 0.3 200 ●

Treatment ●
●
CONTROL
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SALT
AGR (kpixels/day)

150 ● ● 150

TR (mL/day)
●

0.2 ●
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RGR
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0 0
1 2 3 1 2 3 1 2 3
Interval Interval Interval
TPA – Variation in salt tolerance indices across traits and intervals

6
AGR RGR TR
10.0
Interval 6

1
2 7.5
4
3 4

Density

Density

Density
ST1 5.0

2 2
2.5

0 0.0 0
0.25 0.50 0.75 1.00 0.25 0.50 0.75 1.00 1.25 0.25 0.50 0.75 1.00
AGR ST1 RGR ST1 TR ST1

0.05 50 0.08

0.04 40
0.06

ST3 0.03 30

Density

Density

Density
0.04
0.02 20

0.02
0.01 10

0.00 0 0.00
0 50 100 150 200 0.10 0.15 0.20 0.25 0.30 0 50 100 150
AGR ST3 RGR ST3 TR ST3
2.5
2.0 4

2.0
1.5 3

ST6
1.5

Density

Density
Density
1.0 2
1.0

0.5 1
0.5

0.0 0 0.0
0.0 0.5 1.0 1.5 2.0 0.5 1.0 0.0 0.5 1.0 1.5
AGR ST6 RGR ST6 TR ST6
TPA – Interesting correlations between AGR, TR and RGR
TPA – Correlations between traits and different salt tolerance indices vary

ST ST
1 6
TPA – Accessions of interest

60
●
M238

1.0
●
M058
●
M115 ●
M130
50 ●
M275
●
M059

Tissue [Na], salt (mmol/gDM)

●
M017
●
M117 ●
M234
●
M185 ●
M233
●
M043 M292 ●M231
●M207
●
●
M053
●
M044
0.8 ●
M147
●
M112 ●
M081 ●
M190
●
M147 ● M046
M084 ● ●
M050
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M072 ●
M178
●
M082
SFM, salt (g)

40 ● M038
M166 ●
●
M248
●●
●M074
M211
● M209
●
M048 ●
M284
● M171
M133 ● M196 ● M158
●M105
M175
● M176●
●
M113
●
● M160
M140 ●
M273 ●
M157 ●
M176 ●
M088 ●
M046
●
M028
●
M120 ●
M183 ●M080
M167
●
●●
M085
●●M200
M101 M271
M129 ●
●●● M138
M127 ●
●
M211
M252 ● M067
M102 ●
M081
●
M096 ●
M036
● M170
M050
●●
M294 ●●
M197
M191
●
M055 ●
M269
●
● M012
●
M077 ●
M186 ●
M291 0.6 ●
M084 ●
M156
●
M089 M086
M087 ●●
M094
●●● M011 ●
M020
M261
M136 ●
● M080
●
M024 M054 ●M255
M256 ●● M288
M009 ● M264
M022 ●● ●
M156 ●
● ●
M008 ●●●
M286
●●
● ● M125
M030 ● M232
M192 ●M053
●
M033 ●
M112 M130
30 ●
M097 M051 ●M142
M093
M137 ●
M016 M095 ●
M159 ●
M212
●
M201 ● ●
M093M094
●
M070 ●
M167 ●
M052
● M135
M210 ●
M236
●
M207
M221
●
M037 ●
M299 ●
M088 ● ●
M103
●
M169 ● M291
M289
●
M221 ● M001
M237 ●
●M039 ●● M253
M107
M285 ●●
M284 ●M109
M144●●M179 ● ●
M250
M045 ●
M234 ● M231
●
M237
● M151
M247 ●M184
●● M201
M229 ●●
M239
●●●
M079 M060
M075●● M110
●M241
●M076 ●●
M301 ●
M108 ●
M197
●
M269
●
M054
M245
●
M285 ●
M292 ●
M001
●
M289 M199 ●M083
● M228 ● M240● ● M245
M174 ● ●
M010 ●M275
●M166
M003 ●
M250
● ●M033
M035
M258 ●● M276
●M251 ● ●M267
●M181 ●M298
M270 ●
M145 ● ●
M082
●
M125
M021 ●M064
M056 ● M268
M023 M290
●
●
M145 ●
M248
●
M264 ●M200
M187
●
M023
M101
●
M171
●M172
M216 ●● M119
M157
M155 ● M217 ●
M048 ●
M036 ● ●
M110
●M296
● ● ●
M142 ●
M273
●●●M015
M019 ● M013
M018
M227 ●M287
● M187
M099
●
M218
●
M244● M214
●
M189
●
M116 ●
●
M062 0.4 ●
M256 M247
M199 ●
● M287
● ●
M085
●M079
M028
●
●
M020
●
M065 ●
M193 ●
● M229
M253
●
M029 ●
M293
●
M005 ●
M007
20 ●
M034
●●
M225
●M118
M006 ●
● M143
M029
●M104
M141M282
●
M049
●
●● M293 ●●
M078
M002 ●
M217
●
M216
●
M169
●
M034 ●
M301
M040 ● M003
●●
●M198
M226 ● M031
●M057 ●
M223
●
M106 ●
M155
●
M220 ●
M014 ● M078
M106
●
M073 ●
M282
●
●
M297 ●
M177 ●
M224
●
M010 ●
M018
●
M042
●
M066
0.2
10
40 60 80 100 0.1 0.2 0.3 0.4
SFM, control (g) Tissue [Na], control (mmol/gDM)
Chapter 2
Phenotyping the diversity panel
Mature plants, field conditions (Hada al Sham)
Special Acknowledgements

KAU: Prof. Magdy Mousa

Salt Lab: Sónia Negrão, Gabriele Fiene, Sandra Schmöckel, Magdalena Julkowska, Dinara
Utarbayeva
HALO laboratory: Prof. Matthew McCabe, Rasmus Houborg, Samir Al-Mashharawi, Yoann
Malbéteau, Stephen Parkes, Kasper Johansen, Yoseline Angel Lopez, Matteo Ziliani,
Alejandra Pereo Bareto, Christian Andrade Corona, Danqing Huang, Ting Li
Hada al Sham Field Experiment 2016-17 – Site overview

Objective: Phenotyping focusing on fruit- and yield-related

traits in mature plants

Terminal data
• Shoot and root biomass
• Yield
• Fruit

~30m
• Shoot, root and fruit imaging
• General observations

Design
• 4 fields (2C & 2S)
• 300 plants/field
• 230 accessions
• Blocked row and column design, unequally replicated Layout of single field (x4)
Hada 2016-17 – Experimental outline

- Sow in nursery (KAUST greenhouse)

end August
- Transplant to field
early October 3 Oct 2016
- Salt stress application (~60mM)
end October
- Harvest & Phenotyping
early January
19 Nov 2016

10 Dec 2016 8 Jan 2016

Hada 2016-17 – Harvest

Shoot and root mass Shoot Images Root Images

Hada 2016-17 – Harvest

Fruit- and yield-related traits: Immature/mature fruit number/mass, total soluble sugars (TSS), taste…
Hada 2016-17 – Results
0.20 1.2
Treatment 1.00

C
0.15 S 0.9
0.75
Density

Density

Density
0.10 0.50 0.6

0.05 0.25 0.3

0.00 0.00 0.0

0 5 10 15 20 0 1 2 3 4 5 0 1 2 3
SFM (kg) MFY (kg) MFM (g)
0.25

3
1.5 0.20

2 0.15

Density
Density

1.0 Density
0.10

1
0.5
0.05

0.0 0 0.00

0.0 0.4 0.8 1.2 0.0 0.2 0.4 0.6 0.8 0 5 10 15

FMR HI TSS (brix)

MFY: Mature fruit yield MFM: Mature fruit mass FMR: Fruit maturity ratio
HI: Harvest index TSS: Total soluble sugars
Ongoing Hada al Sham field experiment (Hada 2017-18)

Protocol modifications:
• Increased spacing between plants
• Shortened growing season
• Planted fewer accessions
• Remote sensing using drones:
 RGB
Growth rates, biomass…
 Hyperspectral imaging
Chlorophyll, carotenoids, flowering, yield…
 Thermal imaging
Transpiration

In collaboration with Prof. Matthew

McCabe and the HALO laboratory

 Harvest in January
Chapter 3
S. pimpinellifolium reference genome
Sequencing, assembly, annotation, analysis
Special Acknowledgements

CBRC: Salim Bougouffa, Rozaimi Razali, Magbubah Essack, Intikhab Alam, Allan Kamau,

Damien Lightfoot, Sónia Negrão, Stefan Arold, Salim Al-Babili, Yveline Pailles, Mohamme
Shahid, Craig Mitchell, Sandra Schmöckel, Shwen Ho,
Reference genome – Methods
Reference genome – Summary of findings

Summary:
• Improved assembly & annotation (25,970 genes)

• OrthoMCL identifies S.p.-specific genes

• Detected enrichment in stress-related KO

• Discovered increased copy number of I3PS gene

• Performed protein structure analysis of S.p. I3PS

• Explored role of myo-inositol metabolism in salinity-stress

 Manuscript revised and ready to resubmit (pre-print available

on BioRXiv)
Chapter 4
Genotyping and genetic analysis
Genotyping-by-sequencing & population structure
Special Acknowledgements

Cornell Genomic Diversity Facility

Salt lab: Gabriele Fiene, Noha Saber, Octavio Salazar

Genotyping-by-Sequencing

Library preparation

295 DNA samples

230 Unique accessions
65 Replicates

RE: PstI

 Library preparation and

sequencing performed at
Cornell Biodiversity
Institute
Genotyping-by-Sequencing – SNP calling using TASSEL 5

TASSEL 5 GBSv2 in-line command pipeline

 46,450 SNPs
Using default parameters; Unfiltered

Next
• Tweak parameters
• Other pipelines
Fast-GBS, IGST, UNEAK, STACKS…
• Analysis of population structure
Chapter 5
Association study
GWAS and candidate analysis
GWAS – Plans
Marker-by-treatment interaction model
Chapter 6
Side projects
MVApp, DES-TOMATO, Superhydrophobic sand
Special Acknowledgements

MVApp: Dr. Magdalena Julkowska, Stephanie Saade, Ge Gao, Mariam Awlia

DES-TOMATO: Dr. Adil Salhi, Dr. Sónia Negrão, Dr. Magbubah Essack, Dr. Salim Bougouffa, Dr. Rozaimi Razali, Dr.
Aleksandar Radovanovic, Dr. Benoit Marchand, Dr. Maxat Kulmanov, Dr. Robert Hoehndorf, Prof. Mark tester and Prof.
Vladimir Bajic
Superhydrophobic sand: Prof. Himanshu Mishra, Joel Reihmer, Adair Gallo Jr., Prof. Magdi Mousa, Dr. Samir Al-
Mashharawi, Prof. Mark Tester
Side projects
Timeline
Chapter 1  Complete
Chapter 2  Harvest January; Data analysis by April
Chapter 3  Complete
Chapter 4  SNP calling and population structure by February
Chapter 5  GWAS results by May

Graduation by December 2018

Acknowledgements
Salt lab CBRC ICBA
Mark Tester Vladimir Bajic Mohammed Shahid
Sónia Negrão Salim Bougouffa
Sandra Schmöckel Rozaimi Razali KAU
Magda Julkowska Magbubah Essack Magdi Mousa
Yveline Pailles Intikhab Alam & colleagues
Stephanie Saade Allan Kamau
Nadia Al-Tamimi HALO laboratory
Octavio Salazar TPA Matthew McCabe
Helena Oakey Bettina Berger Rasmus Houborg
Gabriele Fiene Lidia Mischis Samir Al-Mashharawi
Noha Saber Nicky Bond Yoann Malbéteau
Lillian Li Fiona Groskreutz Stephen Parkes
Jyoti Dubey Guntur Tanjung Kasper Johansen
Sundus Bukhari Evi Guidolin Yoseline Angel Lopez
Khadija Zemmouri Robin Hosking Matteo Ziliani
Shwen Ho George Sainsbury Alejandra Pereo Bareto
Damien Lightfoot Trevor Garnett Christian Andrade Corona
& Everyone for harvest!! Helli Meinecke Danqing Huang
Richard Norrish Ting Li
Greenhouse
Muppala Reddy Cornell Biodiversity Family & Friends
Gomerito Sagun Institute Sabrina Vettori
Mum and grandparents
Maha Olschowski
Thank you for listening!