Gene Introgression from Crop Wild Relatives into Cultivated Tomato

for Heat Stress Tolerance

Karungan Selvaraj Vijai Selvaraj

1,*

, Karthikeyan J

, Rajiv Periakaruppan

2,*

, Bharathi Ayyarappan

3,*

Irene Vethamoni P

, Manikanda Boopathy N

, Indu Rani C

, Aneesa Rani M. S

and Mutthuvel I

4,*

Vegetable Research Station, Tamil Nadu Agricultural University, Palur, India

Department of Biotechnology, PSG College of Arts & Science, Coimbatore, India

Agricultural College and Research Institute, Tamil Nadu Agricultural University, Eachangkottai, India

Horticultural College and Research Institute, Tamil Nadu Agricultural University, Coimbatore, India

Centre for Plant Molecular Biology and Biotechnology, Tamil Nadu Agricultural University, Coimbatore, India

Horticultural College and Research Institute, Tamil Nadu Agricultural University, Paiyur, India

* * *

Keywords: Tomato, Crop Wild Relatives, Heat Stress.

Abstract: Tomato (Solanum lycopersicum L.) is a crucial vegetable crop worldwide, facing significant challenges due

to climate change-induced heat stress. Elevated temperatures negatively impact tomato productivity by

disrupting various physiological and reproductive processes. To mitigate these challenges, there is increasing

interest in harnessing genetic resources from crop wild relatives (CWRs) through introgression breeding. This

review explores recent advancements in understanding heat stress tolerance mechanisms in tomatoes and the

prospects of introgressing heat tolerance genes from CWRs into cultivated tomato varieties. The complex

responses of tomato plants to heat stress, focusing on reproductive traits, pollen viability, and physiological

and biochemical adaptations are discussed. Additionally, highlight the genetic basis of heat tolerance and the

role of various genes, QTLs, and enzymes in mediating heat stress responses. Furthermore, review emerging

biotechnological approaches, including transcriptomics, proteomics, genome-wide association studies

(GWAS), metabolomics, and advanced imaging techniques, for enhancing heat stress tolerance in tomatoes.

Finally, we address the challenges and opportunities in introgression breeding and emphasize the importance

of utilizing CWRs as valuable genetic resources for developing heat-tolerant tomato varieties

1 INTRODUCTION

Tomato (Solanum lycopersicum L.) is a vital fruit

vegetable crop worldwide, self-pollinating and

diploid with 2n = 24 chromosomes and a genome size

of about 950 Mb (Barone et al., 2008). It boasts a

genetic linkage map and wide germplasm resources

(http://tgrc.ucdavis.edu) and ranks as the world's

second-largest major vegetable commodity. Climate

change, a global threat highlighted by the IPCC

(Leisner et al., 2020, Shahzad et al., 2021),

significantly impacts tomato production, leading to

abnormal price fluctuations. Climate change is

expected to reduce total agricultural crop yields by

4.5 to 9% from 2010 to 2039 (Mahapatra, 2014),

Corresponding Author

affecting plants with abiotic stresses like drought,

heat, cold, salt, and heavy metals (Buono & Regni,

2023). Despite the cultivation of approximately 7500

tomato cultivars, most are susceptible to stress (Singh

et al., 2020). Breeders are increasingly pressured to

enhance stress tolerance using various breeding tools,

with crop wild relatives (CWRs) presenting an

untapped genetic diversity reservoir, especially for

stress tolerance traits (Dempewolf et al., 2017).

Introgression breeding plays a crucial role in

broadening the genetic base and improving stress

tolerance in tomatoes to meet current and future

challenges in crop production.

Selvaraj, K. S. V., J, K., Periakaruppan, R., Ayyarappan, B., P, I. V., N, M. B., C, I. R., M. S, A. R. and I, M.

Gene Introgression from Crop Wild Relatives into Cultivated Tomato for Heat Stress Tolerance.

DOI: 10.5220/0012882200004519

Paper published under CC license (CC BY-NC-ND 4.0)

In Proceedings of the 1st International Conference on Emerging Innovations for Sustainable Agriculture (ICEISA 2024), pages 78-85

ISBN: 978-989-758-714-6

2 IMPACT OF HEAT STRESS

Tomato growers struggle with heat-sensitive

cultivars, exacerbating vulnerability to rising

temperatures. High temperatures hinder tomato

growth and yield by disrupting various biological

processes, resulting in decreased productivity

(Gonzalo et al., 2020). A 2-4°C temperature rise

disrupts gamete development and flower maturation,

reducing seed yield (Solankey et al., 2018). Tomato

heat tolerance, a complex trait, links to flower

structure and metabolic processes, impacting proline,

polyamine, and carbohydrate levels (Alsamir et al.,

2017a; Sato et al., 2006; Song et al., 2002). Yeh et al.

(2012) identified four primary thermo-tolerance

categories in tomatoes: short-term acquired

thermotolerance, long-term acquired

thermotolerance, basal thermotolerance, and

thermotolerance to moderately high temperatures.

Heat stress response in tomatoes is genotype and

developmentally dependent, altering gene expression

in post-anthesis fruit (Gonzalo et al., 2021).

2.1 Pollen Viability

Heat stress affects pollen viability in anthers, crucial

for fruit setting (Alsamir et al., 2017a). High

temperatures emphasize the importance of pollen

viability for fruit setting, showing a consistent

positive correlation in studies (Zhou et al., 2015).

Tomato studies show heat stress lowers pollen

viability and quantity, highlighting genotype

selection for heat tolerance (Xu et al., 2017a;

Driedonks et al., 2018a). Metabolites like proline,

glutathione, phytohormones, flavonoids, polyamines,

and carbohydrates impact pollen survival in heat

stress, showcasing intricate biochemical regulation

(Paupière et al., 2014). Advancements in high-

throughput phenotyping, like image analysis and

impedance flow cytometry, automate pollen number

and viability analysis, aiding in efficient heat stress

assessment (Dreccer et al., 2019). Open-access

image-based tools, such as Pollen Counter, enhance

accessibility and accuracy in pollen counting and

viability assessment (Tello et al., 2018).

2.2 Physiological and Biochemical

Trait

Physiological and biochemical responses to high

temperature stress are vital indicators of plant stress

tolerance, impacting health and productivity (Zhou et

al., 2019). Maintaining optimal carbohydrate levels,

chlorophyll content, and photosynthetic efficiency is

crucial for pollen quality and plant performance

during heat stress (Firon et al., 2006). Segregating

generations reveal complex genetic basis for traits

like chlorophyll content and PSII's quantum

efficiency (Fv/Fm) (Wen et al., 2019). Metabolite

profiling aids thermotolerant resource identification,

enhances breeding efficiency (Raja et al., 2019;

Driedonks, 2018; Mazzeo et al., 2018). Soluble

sugars affect anther & pollen development.

Thermotolerant types have more fructose & glucose

(Raja et al., 2019; Driedonks, 2018; Mazzeo et al.,

2018). Compounds like proline, glycine betaine,

flavonoids, jasmonic acid, and indole-3-acetic acid

affect fruit set, pollen fertility, and stress tolerance in

plants through osmotic adjustment (Hungria and

Kaschuk, 2014; Giri, 2013). Heat stress reduces

photosynthesis, stomatal conductance, and membrane

stability in tomatoes, correlating with decreased

inflorescence, pollen viability, and fruit setting

(Hungria and Kaschuk, 2014; Giri, 2013). Plants

adapt to heat stress through biochemical and

physiological changes, aiding crop heat tolerance

enhancement via breeding and management.

Mechanisms like carbohydrate regulation,

chlorophyll maintenance, and osmotic adjustment

offer pathways for improvement. Metabolite profiling

and genetic studies aid in identifying thermotolerant

genetic resources and targeted breeding strategies.

3 CROP WILD RELATIVES

(CWRs) RESERVOIR FOR

CROP IMPROVEMENT

Crop wild relatives (CWRs) are vital genetic

resources for crop improvement, offering ancestral

diversity for domesticated crops (Choudhary et al.,

2017). Wild tomato relatives provide useful traits for

breeding (Olivieri et al., 2020; Dempewolf et al.,

2017). Wild tomato species vital for heat tolerance

due to important genes (Zhang et al., 2017). An

introgression population of Solanum neorickii is

recognized as a potent complement to the extensively

examined Solanum pennellii (Brog et al., 2019).

Recent studies have assessed the genetic variability in

a panel of cultivated and wild tomatoes with varying

levels of heat tolerance using genomic and

phenotypic analysis (Ayenan et al., 2021). Long-term

mild heat stress studies on wild tomato species, like

S. pimpinellifolium, highlight their adaptive potential

for heat stress, aiding local adaptation (Driedonks et

al., 2018).

Gene Introgression from Crop Wild Relatives into Cultivated Tomato for Heat Stress Tolerance

Table 1: Enzyme involved in heat stress tolerance.

Enzyme Function Reference

Heat Shock Proteins

(HSPs)

Chaperone proteins aid protein folding during heat

stress

Wang et al.

(2004)

Superoxide Dismutase

(SOD)

Antioxidant enzymes combat superoxide radicals

in heat stress

Mittler et al.

(2012)

Catalase (CAT) Antioxidant enzyme breaks down hydrogen

peroxide into water and oxygen

Hasanuzzaman et

al. (2019)

Glutathione

Peroxidase (GPX)

Antioxidant enzyme catalyzing the reduction of

dro

eroxide and or

anic h

droperoxides

Foyer and Noctor

(2011)

Heat Shock Factor

(HSF)

Transcription factor controls heat shock protein

expression durin

hea

stress

Kotak et al. (2007)

Ascorbate Peroxidase

(APX)

Antioxidant enzyme uses ascorbate to neutralize

dro

eroxide

Sharma et al.

(2012)

3.1 Introgression

Introgression, a genetic phenomenon characterized

by the transfer of genetic material between species

through repeated backcrossing, offers a pathway for

enhancing heat tolerance in tomatoes. Introgression

from Solanum pimpinellifolium enhances heat

tolerance in tomatoes by expanding genetic diversity,

enabling breeding of thermo-tolerant varieties

(Ayenan et al., 2021). Additionally, investigation

finds heat-tolerant tomato E42's genome linked to

wild S. pimpinellifolium, revealing 35 key adaptation

genes (Graci et al., 2023). Heat-tolerant genotypes

enhance fruit quality via backcross hybridization

(Ibrahim, 2016). Tolessa et al. (2013) studied tomato

introgression lines from S. esculentum and L.

chmielewskii, examining pollen viability and fruit set

under moderate heat. Kubond et al. (2023) found

positive effects of S. habrochaites alleles on tomato

traits via trait-genomic region associations,

suggesting potential for improving fruit quality in

cultivated tomatoes. However, Poudyal et al. (2017)

demonstrated that using Solanum habrochaites

rootstock boosts tomato yield in cold/drought. Vitale

et al. (2023) found that Solanum pennellii IL12-4-SL

outperformed M82 in heat tolerance, showing more

flowers, better pollen, and sustained photosynthesis

under stress.

Figure 1: Impact on heat stress tolerance.

ICEISA 2024 - International Conference on ‘Emerging Innovations for Sustainable Agriculture: Leveraging the potential of Digital

Innovations by the Farmers, Agri-tech Startups and Agribusiness Enterprises in Agricu

Table 2: CWRs for heat stress tolerance

Wild relatives Reference

S. pennellii Gonzalo e

al., 2021

S. pimpinelli

olium Gonzalo e

al., 2021

S. cheesmanii Golam, F e

al., 2012

S. chmielewskii

ahar, K. e

al., 2011

S. peruvianum Driedonks e

al., 2018

3.2 Challenges in Introgression

Despite the sterility of progenies, linkage drag, and

self-incompatibility in wild tomatoes, various

techniques have been developed to broaden the

genetic base of cultivated tomatoes (96). These

techniques include embryo rescue, advanced

backcross QTL analysis, chromosome segment

substitution lines (CSSL), backcross inbred lines

(BIL), and introgression lines (ILs), targeting linkage

drag (Tanksley et al., 1996; Ali et al., 2010; Bessho-

Uehara et al., 2017). For instance, studies have

demonstrated the potential for creating hybrid S.

lycopersicum × S. sisymbriifolium and S.

lycopersicum × S. peruviyanum plants through

embryo rescue techniques, showcasing the

effectiveness of these methods in overcoming

breeding barriers and expanding genetic diversity in

tomato breeding programs (Piosik et al., 2019).

3.3 Genes and QTLs for Heat Stress

Tolerance

Tomato heat tolerance traits influenced by additive,

dominant, and epistatic gene effects, varying with

germplasm (Dane et al., 1991). Research finds genes

& QTLs linked to heat tolerance in tomatoes, aiding

breeding. Traits like inflorescence count, pollen

viability, and others show additive & dominance QTL

effects, with additive effect more significant (Xu et

al., 2017b; Driedonks et al., 2018). Although QTL

linked to tomato performance under heat stress were

found by several studies, their applicability for

breeding was limited due to the lack of mapping onto

chromosomes. Conversely, QTL linked to traits

related to heat tolerance were discovered by Xu et al.,

(2017b); Driedonks, (2018); Wen et al., (2019).

Assessment of high-temperature stress on tomato

yield, identification of stable genotypes, and analysis

of QTL and transcriptome changes related to heat

response were conducted (Bineau et al., 2021).

Conventional QTL mapping, QTL-seq, and RNA-seq

were used to pinpoint heat-tolerance QTLs and stress-

responsive genes, expediting breeding for heat-

tolerant varieties (Wen et al., 2019). Study found

genetic basis of heat tolerance in tomato reproductive

traits, identifying QTLs, including one for pollen

viability (Xu et al., 2017). Genome-wide association

studies on tomato genotypes in control and high

temps pinpointed heat tolerance genes, emphasizing

markers for inflorescence and fruit traits (Alsamir et

al., 2019). Research identifies genes & QTLs for heat

tolerance traits in tomatoes using QTL mapping,

QTL-seq, RNA-seq & GWAS, aiding breeding of

resilient varieties.

Figure 2: Backcross Breeding

Gene Introgression from Crop Wild Relatives into Cultivated Tomato for Heat Stress Tolerance

Table 3: Gene/Locus involved in Heat stress tolerance.

Gene/Locus

Symbol

Function Related Trait /

Phenotypes

References

SOD Antioxidan

enz

me Antioxidan

defense Zhou e

al., 2019

APX Antioxidant enzyme Antioxidant defense Zhou et al., 2019

SENU3

Senescence-associated

cysteine

roteinase

Leaf senescence

Drake et al., 1996; Xiao

et al., 2014

HsfA1 a, b, c, d Transcriptional activators to

Transcription

regulatory network

EI - Shershaby et al.,

2019

HsfB1 Later gene in transcription

ulator

networ

Transcription

ulator

networ

EI - Shershaby et al.,

2019

TTS, TGL11 Pistil-specific expression Flowe

morpholo

Mülle

al., 2016

TAP3, TM6, PI Class B activit

Flowe

morpholo

Mülle

al 2016

CLV Signal peptide, shoot, and

floral meriste

ulation

Shoot and floral

meriste

Fletcher, 2018; Quinet et

al., 2019

WUS Homeodomain transcription

factor, shoot and floral

meristem re

ulation

Shoot and floral

meristem

Fletcher, 2018; Quinet et

al., 2019

3.4 Emerging Techniques

Recent advancements in transcriptomics and

proteomics have enabled researchers to identify key

genes and proteins involved in tomato's response to

heat stress. For example, Tian et al. (2021) analysed

heat-stressed tomato plants' gene expression,

revealing heat tolerance-related gene changes.

GWAS identified genetic loci linked to heat stress

tolerance in tomatoes, aiding in pinpointing candidate

genes for validation. For instance, Ruggieri et al.

(2018) GWAS links heat tolerance genes in tomatoes.

Metabolomic studies reveal metabolic changes and

potential biomarkers under heat stress.

4 CONCLUSION

The Research on heat stress tolerance in tomatoes

should focus on genetic basis and mechanisms,

utilizing biotechnological tools like gene editing and

GWAS. Improving introgression breeding methods

from crop wild relatives is vital. Collaboration among

researchers, breeders, and farmers is key for

validating and deploying heat-tolerant varieties.

Addressing socio-economic factors is crucial for

global impact on food security and sustainability.

Tomato breeding for heat stress promises resilience

amid climate change.

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Gene Introgression from Crop Wild Relatives into Cultivated Tomato for Heat Stress Tolerance