improving coffee species for pathogen resistance · breeding varieties that are resistant to a...

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CAB Reviews 2020 15, No. 009

Improving coffee species for pathogen resistance

Fatemeh Maghuly1*, Joanna Jankowicz-Cieslak2, and Souleymane Bado1,3

Address: 1Plant Functional Genomics, Department of Biotechnology, BOKU-VIBT, University of Natural Resources and Life Sciences, Vienna, Austria 2Plant Breeding and Genetics Laboratory, International Atomic Energy Agency, Vienna, Austria 3Deptartment of Plant Science, PHYTOPRISE GmbH, Oberwart, Austria

*Correspondence: Fatemeh Maghuly. Email: [email protected]

Received: 02 July 2019Accepted: 15 January 2020

doi: 10.1079/PAVSNNR202015009

The electronic version of this article is the definitive one. It is located here: http://cabi.org/cabreviews

© CAB International 2020 (Online ISSN 1749-8848)

Abstract

Pathogens are the major limiting factors in coffee productions. Approximately 26% of the global annual coffee production is lost due to diseases, threatening the income of nearly 125 million people worldwide. Therefore, reducing coffee yield losses by improving the resistance of coffee plants to disease and insect attack will provide a major contribution to agricultural sustainability and disease management of many regions. Breeding varieties that are resistant to a broad spectrum of pathogens, genetically stable and high yielding, requires strategies that will overcome challenges known by coffee breeders. Recently developed genomic tools allow a better understanding of coffee-pathogen interaction and help to identify genes involved in pathogen resistance or susceptibility. Understanding the influence of individual factors and their interaction will help to select interesting accessions and to accelerate breeding strategies for coffee improvement. Additional information on the quantitative effect of pest and disease on coffee crop losses and the understanding of their impact are essential to develop the best pest management strategy. This review provides an overview of the current knowledge of coffee production and recent advances in resistance breeding programs, with emphasis on induced mutagenesis, genomic tools, and genome editing. The focus is on the origin, domestication, evolution, and gene pools of coffee. Moreover, answers will be given toward: how we can benefit from establishing a genetically diverse coffee population; how genomic resources can play an important role in host resistance; and what are the major pathogens affecting coffee.

Keywords: resistance breeding, CC-NBS-LRR receptors, resilience, marker-assisted selection (MAS), R genes, mutation breeding

Review Methodology: Searches used different websites including Web of Knowledge (https://apps.webofknowledge.com/), Scopus (https://www.scopus.com/), The International Coffee Organization (ICO, http://www.ico.org/), FAOSTAT (http://www.fao.org/faostat/), Plant breeding and genetics (http://www-naweb.iaea.org/nafa/pbg/index.html), FAO/IAEA officially released mutant database (https://mvd.iaea.org). The following keywords were used in searches: major diseases, resistance breeding, mutation breeding, new plant breeding techniques, mutation induction, vegetative propagated, economic impacts, genomic tools, and genome editing.

Origin, domestication, evolution, and gene pools of coffee

Coffee is a member of the Rubiaceae family, Eusterid I clade and the fourth largest family of angiosperm, containing 124 species spread across two genera, Coffea and Psilanthus. Cultivated coffee originated from wild populations in Africa, Madagascar, the Comoros Islands, Mascarene Island,

Indian subcontinent, south tropical Asia, south-eastern Asia, and Australasia [1–5]. Previous phylogenetic studies based on rDNA, cpDNA, and sequence data divided genus Coffea into four groups with different geographic origins in Africa clades (Central and Western, Eastern, Central African) and the Madagascar clade [5–11]. Davis et al. [5] distributed the pattern of Coffea variation into six main lineages, containing: a) African “Psilanthus” clade, b) Asian

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https://protect-eu.mimecast.com/s/XCPbCy9y6TjJjyHZktpT?domain=apps.webofknowledge.com

https://protect-eu.mimecast.com/s/hK2qCz7zBcPnPmSXMCtK?domain=scopus.com

https://protect-eu.mimecast.com/s/dafeCAMlQHmVm1C9VEma?domain=ico.org

https://protect-eu.mimecast.com/s/b40XCBPm8CZAZlHjHYob?domain=fao.org

https://protect-eu.mimecast.com/s/OIXFCDQoYf6M6OCleHQq?domain=www-naweb.iaea.org

https://protect-eu.mimecast.com/s/oKP5CE0pZUAnA6tQahYX?domain=mvd.iaea.org

https://protect-eu.mimecast.com/s/oKP5CE0pZUAnA6tQahYX?domain=mvd.iaea.org

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and Australasian “Psilanthus” clade, c) the lower Guinea/Congolin clade (e.g., C. liberica and C. canephora), d) the Upper Guinea clade with the Ease-central African clade (e.g., C. anthonyi), e) the Indian Ocean clade, and f) the dry-adapted Madagascan with an East African clade. The study by Razafinarivo et al. [1] using SSR data showed that speciation in East Africa, Madagascar, and Mascarenes might have occurred later in Western and Western-Central Africa, which is not in agreement with the distribution of genome size. All species of Coffea analyzed for ploidy level are diploid (except C. arabica) and have the same number of chromosomes with differences in genome size. The largest genome size belongs to Western and Western-Central African species (1.52 pg/2C), while the smallest belongs to Eastern African (1.21 pg/2C) and Mascarene species (1.19 pg/2C). It was reported that diversification in subgenus Coffea most likely occurred in 450,000–100,000 years BP [8, 12, 13].

Among different coffee species, the two economically most important are the diploid C. canephora Pierrre ex Froehn (2n=2x=22), native to Central and Western sub-Saharan Africa, and the allotetraploid C. arabica L. (2n=4x=44), which is native to southwestern Ethiopian highlands, Mount Marsabit of Kenya, and the Boma Plateau of Sudan [14, 15]. C. arabica resulted from ancestral hybridization between two diploid ecotypes of C. eugenioides S. Moore and C. canephora, dated back approximately 50,000 years [8, 12, 13]. It is self-pollinated, similar to two other diploid species, C. heterocalyx Stoff. and C. anthonyi Stoff. & F. Anthony, while C. canephora is cross-pollinated. Arabica coffee is cultivated under shade and at a high altitude of 1400–1800 m above sea level. The recent study by Sant’Ana et al. [16] showed a high allelic variation in wild accessions from Ethiopia, whereby, the mode of pollination and the history of coffee cultivation resulted in a reduction of genetic diversity in C. arabica. According to different authors, coffee was introduced from Ethiopia to Yemen between 1500 and 300 years ago. From this point, the first reduction of diversity happened within Arabica cultivars. Genetic data analysis showed that two genetic bases spread from Mocha (Yemen) in the

early eighteenth century [17, 18]; C. arabica var. arabica (usually called C. arabica var. typica Cramer) originated from a single plant that was introduced to Java (Indonesia) and later cultivated in the Amsterdam botanical gardens; and C. arabica var. bourbon (B. Rodr.) Choussy [19, 20] was introduced to the Bourbon Island (Réunion). These were the starting points for the spread of coffee cultivars rapidly to the American continent and Indonesia using seeds produced by auto-fertilization of coffee trees, causing further reduction in genetic diversity.

Besides these two important economic coffee species (C. canephora and C. arabica), other minor species are also used for commercial or breeding purposes. These include C. liberica Hiern, C. eugenioides, C. dewevrei De Wild. & T. Durand, C. stenophylla G. Don, and C. racemose Lour., which carry valuable sources of disease resistance [21].

World coffee production

After petroleum, coffee beans are the second most economically important product traded worldwide [22]. With approximately 2.25 billion cups of coffee consumed daily in the world, coffee production provides income to around 125 million people in developing countries. Nowadays, approximately 11 million hectares of coffee trees are cultivated in tropical regions [23].

The Food and Agriculture Organization Statistics (FAOSTAT) database (2018) estimated that more than 9,221,534 tons of green coffee beans were produced worldwide in 10,975,184 ha in 2016. America with an average production of 4,416,981.83 tons (57.7%) is the largest coffee producer in the world, followed by Asia (27.2%) and Africa (14.2%) (Fig. 1). It is also reported that Brazil, Vietnam, and Columbia with an average production of 2.2, 0.9, and 0.66 million tons, respectively, are ranked as the top three coffee-producing countries worldwide (Fig. 2). Indonesia and India are the second and third largest producers in Asia with 0.6 and 0.28 million tons of green coffee beans,

Figure 1. Production share of green coffee by regions (FAOSTAT Databases, 2018).

Fatemeh Maghuly, Joanna Jankowicz-Cieslak, and Souleymane Bado 3


respectively, in 2016. However, the production of green coffee beans is still low in many Asian countries. From African countries, only Ethiopia with 0.27 million tons ranked in the top 10 coffee producers worldwide (FAOSTAT, 2018). Figure 3 shows world area harvested and production of green coffee beans (tons) from 1994 to 2016. C. arabica and C. canephora account for about 64% and 35% of the world’s coffee production, respectively [24].

Except for 2003, 2005, and 2011, coffee production has increased continuously worldwide, and the demand for coffee is also growing considerably (0.1% per year). However, global coffee production is at risk, and approximately one-third of the worldwide production is lost annually due to

diseases and pests [25], which also reduce the quality of harvested seeds and its market value.

The International Coffee Organization (ICO, http://www.ico.org/) estimated the global coffee production at 158.56 million bags in 2018, a yield which is 0.3% lower than in 2016/2017. Moreover, in June 2018, ICO reported a 2.6% decrease in the price of coffee (an average of 110.44 US cent/Ib), which was the lowest monthly average since December 2013. Furthermore, ICO reported a decrease in world export, with 9.27 million bags in May 2018, compared to 10.59 million bags in May 2017, resulting from a 32.5% decrease of coffee shipments from Brazil, 25.7% from Honduras, and 55.2% from Indonesia. Interestingly,

Figure 2. Production of green coffee: top 10 producers (FAOSTAT Databases, 2018).

Figure 3. Worldwide production/yield of green coffee (FAOSTAT Databases, 2018).

http://www.ico.org/

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the ICO reported that the most substantial month-by-month drop occurred for Brazilian Naturals, which fell by 0.9% to 118.76 US cents/lb, while the monthly average for Robusta increased by 0.1% to 88.31 US cents/lb.

Decrease in coffee export in the case of 3 out of 10 largest coffee producers was explained by an off-year of the biennial production cycle for C. arabica. This was also related to the amount of rain, the increase in coffee consumption in producer countries, the strengthening of the currencies of South American countries against the US dollar, as well as time needed to recover after an outbreak of coffee diseases, for example, leaf rust (ICO 2018). Based on ICO estimation, a higher coffee harvest was expected for 2018/19, given the fact that C. arabica production will be in an on-year and weather conditions are expected to be beneficial for coffee bean production. A biennial pattern of coffee production and the presence of pests and diseases make assessments of yield loss in a perennial crop such a coffee difficult. Average of yield losses strongly depends on the occurrence and severity of diseases, appearance of multiple pathogens in the same field, as well as environmental conditions, lack of natural enemies, level of plant resistance, and the stage at which infection occurs [26]. Moreover, various diseases may occur at the same time in the same field, which may significantly increase yield losses [27]. Some pathogens, such as nematodes, can survive in the field for years, while others can be transmitted through contaminated seeds (as in the case of coffee berry borer). Above all, it should be considered that due to the fluctuation of price and export changes, coffee farmers struggle between price and production costs. This is especially critical for farmers for whom coffee is the only source of revenue [28]. Day workers are also affected, which results in food stress and insecurity [26]. Therefore, a stable evaluation of production and quantitative information about yield losses of coffee is an essential step to make a better decision for integrated pest management and to make a better evaluation of the effectiveness of pest and disease regulation [25].

Major coffee diseases

Several insects, bacterial, fungal, and viral diseases (Table 1) attack the coffee plant [49, 50].

Among fungal diseases, the coffee leaf rust (CLR, or orange rust), the coffee berry disease (CBD), and coffee wilt disease (CWD) caused by the fungus Hemileia vastatrix, Colletotrichum kahawae, and Gibberella xylarioides, respectively, are problematic in tropical coffee-growing environment and the major cause of coffee yield losses.

There are some economically less important fungal diseases [51] such as Powdery and Yellow Rust or Grey Rust, caused by the fungus Hemileia coffeicola, and Fusarium stilboides (telemorph: Gibberella stilboides), respectively, which are the causal agents of the coffee bark disease. Furthermore, the American leaf spot of coffee incited by Mycena citricolor was reported only on the American

continent in cold, moist areas at higher altitudes [52–56]. Leaf blight: coffee (Phoma costaricensis) is a soil fungus that can attack coffee leaves and fruits, before fruit ripening. It prefers cold, humid, and windy climates. The brown eye spot (Mycosphaerella coffeicola) fungus can also attack leaves and fruits of coffee [48].

In relatively cool regions, two bacterial coffee diseases were reported that may cause severe yield losses: the bacterial halo blight (BHB) caused by Pseudomonas syringae pv. garcae [57] and the coffee leaf scorch (CLS) caused by the polyphagous bacterium Xylella fastidiosa [39]. BHB was reported to cause higher incidence and severity in coffee plantations [53, 59] compared to X. fastidiosa transmitted by the sharpshooter leafhopper Dilobopterus cortalimai (Cicadellidae: Cicadellinae) [60, 61]. Furthermore, it is believed that X. fastidiosa strains are responsible for severe economic losses in South America [62].

Some virus diseases have also been reported in coffee, for instance, coffee ringspot virus (CoRSV), transmitted by mites Brevipalpus Phoenicis (Geijskes), belonging to the family Rhabdoviridae [40]. This usually showed no significant economic impact [53]; however, in 2003, some large-scale infections of CoRSV in Minas Gerais resulted in high yield loss [63].

Root-knot nematodes (RKN, Meloidogyne spp.), and the plant-parasitic nematodes Pratylenchus coffea, and Radopholus arabocoffeae, infect several plant species and cause major damage to cultivated woody species [64]. So far, 12 species of RKN have been described in coffee (M. arabicida, M. izalcoensis, M. konaensis, M. paranaensis, M. coffeicola, M. africana, M. incognita, M. arenaria, M. javanica, M. hapla, M. enterolobii, and M. exigua) [65]. Among them, M. exigua, M. incognita, and M. paranaensis are the most damaging species, causing severe agronomic constraints to coffee plantations due to their wide distribution [66]. M. incognita has the most significant impact in Central and South America, Africa, and Asia. M. exigua was discovered in Rio de Janeiro and later in all coffee-producing countries in America [67, 68].

Among insects threatening coffee production, coffee berry borer (CBB) Hypothenemus hampei (Coleoptera: Curculionidae: Scolytinae) [50] and Antestiopsis Leston (Hemiptera: Pentatomidae) are well known. They not only damage the plants but also contaminate the beans with chemicals that destroy the quality of finished beverage. Unfortunately, the beetle bores into the coffee fruit and lays eggs in the seed endosperm, and, therefore, it is difficult to control them by insecticides. The best strategy to control infections is to prune the tree and remove all coffee fruits after harvesting. Alternative pest management strategies using natural enemies, like parasitoid wasps, or entomopathogenic fungi, can provide some degree of protection; however, their establishment in the field is difficult.

The leaf miner (Perileucoptera coffeella) is a specialized parasite of Coffea species, leading to the reduction of the foliar surface and finally the leaf will fall off [69]. If not controlled, it may cause intense defoliation and loss of production. The coffee white stem borers (CWSBs) of the Cerambycidae family are severe pests of C. arabica in Africa



Table 1. The list of the major disease and pathogens of coffee.

Common nameScientific name (EPPO code) Abbreviation Affected part Host plant Reference

Fungal diseasesAnthracnose Glomerella cingulata (GLOMCI)

Colletotrichum gloeosporioidesBerry C. arabica CABI*, [29, 30]

Leaf blight of coffee Ascochyta tarda leaf C. arabica CABIBlack root rot Rosellinia spp. Root C. arabica CABI, [31]Brown eye spot of

coffeeMycosphaerella coffeicola

(CERCCO)Cercospora coffeicola

Leaf, berry C. arabicaC. canephora

CABI, [32, 33]

Ceratocystis blight Ceratocystis fimbriata (CERAFI)

Xylem C. arabicaC. canephora

CABI

Coffee berry disease

Colletotrichum kahawae CBD Berry C. arabica [32–34]

Coffee wilt disease Gibberella xylarioides (GIBBXY)

Fusarium xylarioides

CWD Xylem Coffea sp. CABI, [32, 33, 35]

Pink disease Erythricium salmonicolor (CORTSA)

Phanerochaete salmonicolor

Stem Coffea sp. CABI, [32]

Coffee leaf rust Hemileia vastatrix (HEMIVA) CLR Leaf C. arabicaC. canephora,

C. liberica

CABI, [32, 33]

Powdery rust of coffee

Hemileia coffeicola (HEMICO) Leaf C. arabicaC. canephora

CABI

Thread blight Corticium koleroga (CORTKO) Leaf, berry, twig

C. arabicaC. canephora

CABI, [36]

Ceratocystis blight Ceratocystis fimbriata (CERAFI)

Xylem C. arabicaC. canephora

CABI

Bark disease: coffee

Gibberella stilboides (GIBBST)Fusarium stilboides

Bark, stem C. arabica CABI, [33]

Leaf blight: coffee Phoma costarricensis (PHOMCO)

Leaf, berry Coffea sp. CABI

Tea root rot Ganoderma philippii (GANOPH)

Root Coffea sp. CABI

America leaf spot Mycena citricolor(MYCECI)Omphalia flavidaStilbum flavidum

ALS Leaf C. arabica CABI

Armillaria root rot Armillaria mellea Root C. arabicaC. canephora

CABI

Bacteriacoffee leaf scorch Xylella fastidiosa (XYLEFA) CLS Xylem Coffea sp. CABI, [37]Bacterial halo blight Pseudomonas syringae

(PSDMGC)BHB Leaf Coffea sp. CABI, [37]

Nematodes, parasiticRoot-knot

nematodeMeloidogyne spp. RKN Root C. arabica CABI, [33, 38]

Root-lesion nematode

Pratylenchus brachyurus (PRATBR)

Root C. arabica CABI, [39]

Viral diseasescoffee ring spot

virusBrevipalpus phoenicis

(CORSV0)CoRSV Leaf, berry C. arabica CABI, [40]

InsectsCoffee berry borer Hypothenemus hampei

(STEHHA)CBB Berry C. arabica

C. canephoraCABI, [33]

Antestia bug Antestiopsis intricate (ANTEIN) AB Berry C. arabica CABI, [41]

Continued

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(Monochamus leuconotus), Southeast Asia, and India (Xylotrechus quadripes), increasing fragility in the plant.

One of the severe pests of C. canephora is black twig borer (Xylosandrus compactus), which is native to Asia but spreads to coffee-growing regions and therefore attacks C. arabica as well. The coffee tree will be damaged by tunneling and introduction of secondary pathogens, like the ambrosia fungus. Infections can be limited through proper plant pruning to reduce the shade [70].

Breeding for resistance to fungal diseases

Infection of coffee plants with H. vastatrix leads to the rust disease. This rust was first observed in 1861 near Lake Victoria, which broke out in Ceylon in 1868, and is now spread throughout coffee-growing countries, causing significant economic impact, plant damage, and yield reduction in the infected field [21, 26, 49]. As reported by ICO (2014), infection of rust has resulted in a loss of 616 Million US Dollars and of 374 000 jobs in Central America.

Genetic studies designated at least nine dominant resistance genes (SH1–SH9) in Coffea, either singly or in combination, conferring coffee resistance to rust, correlated to virulence genes (V1–V9) in the pathogen [21, 71]. So far, in C. arabica four resistance genes were identified (SH1, SH2, SH4, and SH5), which were overcome by the appearance of new rust races carrying new virulence genes. Gene SH3 possibly comes from C. liberica, and the others (SH6, SH7, SH8, and SH9) originate from C. canephora. Among them, SH3, SH6, and SH9 presented durable resistance in coffee plants [71].

In the early breeding programs, Hibrido de Timor (HDT) and Indian selection (e.g., S26), which are tetraploid plants, were used as the primary source of rust resistance [54]. Using AFLP markers for self-pollinated lines S26 (a spontaneous hybrid of C. arabica and C. liberica) and S288, Prakash et al. [72] identified 21 markers tightly linked to the SH3 gene. Of these, one M8 marker co-segregated perfectly with SH3 resistance gene. Later on, Mahé et al. [73] developed six SCAR and three SSR markers co-segregating with SH3 gene, of which two markers (Sat244 and BA-124-12K) were found very closely associated with the SH3 gene, one (BA-48-21OR) located upstream of the SH3 gene (0.6 cM) and one (SP-M16-SH3) located downstream of the gene (1.8 cM). Furthermore, SP-M16-SH3, Sat24, and BA-48-21OR markers allow distinguishing homozygous and heterozygous individuals for the SH3 gene [71, 74]. Physical map of the locus SH3 was completed, and an 800-kb region that covers this locus was sequenced and annotated [75]. Furthermore, the physical location of SH3 locus was detected using in situ hybridization (FISH), localizing it distally on a chromosome of homologous group 1 [76]. In order to understand the genomic organization of locus SH3, Ribas et al. [12] sequenced this region in two subgenomes, C. arabica (Ea, Ca) and one C. canephora (Cc), which represent five, three, and four R genes, respectively. These are related to the CC-NBC-LRR gene family. Since polymorphism identified in the LRR region of the R genes could be related to the resistance to particular pathogens [77], it is possible to transfer R gene from one plant to another to produce a resistant plant against a specific pathogen. Although genetic control of the disease can be useful, effective disease resistance is short-termed, due to fast emergence

Common nameScientific name (EPPO code) Abbreviation Affected part Host plant Reference

White coffee stem borer (Africa)

Monochamus leuconotus WCSB Vascular system

C. arabica [33, 42]

White coffee stem borer (Asia)

Xylotrechus quadripes WCSB Stem C. arabica [43]

Coffee berry moth Prophantis adusta CBM Berry C. arabica [44]Mealy bug Pseudococcus spp. (PSECSP) RMB Leaf, berry,

flower bud, apical shoot

C. arabicaC. canephoraC. eugenioides

CABI, [33]

Green scale Coccus viridis GS Main leaf vein C. arabicaC. canephora

CABI, [33, 44]

Coffee leaf miner Perileucoptera coffeella (LEUCCO)

Leucoptera coffeella

CLM Leaf C. arabica CABI, EPPO

Black coffee twig borer

Xylosandrus compactus (XYLSCO)

BCTB Twig C. arabicaC. canephora

EPPO, [45–47]

Algae

Algal spot of coffee Cephaleuros virescens (CGVEI)

Leaf C. arabica CABI, [48]

*https://www.cabi.org/isc/datasheet/14791.

Table 1. Contiuned.



of new races and high variability. So far, more than 50 races of H. vastatrix were reported [78]. However, the increasing number of infectious plant diseases makes the development of superior cultivars necessary.

The dominant gene race-specific resistance to the pathotype of race II of H. vastatrix was characterized in HDT (UFV 427-15). It carries a dominant monogenic resistance by de Brito et al. [79]. They used 176 AFLP primer combinations and identified 3 markers linked to SH3 resistance gene, 2 markers were distributed in flanking the site of resistance gene. Later, Diola et al. [80] identified the resistance gene in a F2 population from a cross between resistant HDT (UFV 427-15) and susceptible yellow Catuai IAC 30. Further, they developed a high-density genetic map using six SCAR markers, which identified a chromosomal region of 9.45 cM and gene resistance to the pathotype of race II of H. vastatrix (SH?), where the gene was localized within 0.7 and 0.9 cM (loci CaRHvII 1533 and CaRHvII 3459, respectively). Prakash et al. [74] were also able to determine the presence and absence of the SH3 gene using two SCAR markers closely linked to the SH3 gene in two cultivars (S795 and S26), which was the first successful study for marker-assisted selection (MAS) in achieving durable rust resistance. Recently, Alkimim et al. [71] applied MAS for maintenance breeding and gene pyramiding of reaching host resistance to multiple fungal diseases in coffee. They used molecular markers (identified previously) linked to rust resistance genes (SH3 and SH?), and CBD resistance gene (Ck-1) to identify C. arabica genotypes containing resistance genes introgressed from other coffee species.

The other limiting factor of C. arabica production is CBD, infecting all stages of the plant from the flower to ripe fruits and leaves, which may cause up to 50%–60% of crop losses [81]. Although CBD is only reported in Africa, there is some concern for the possible infection in Asia and America, where CBD still did not appear, but the climate is favorable. In 1980, van der Vossen and Walyaro [82] identified genes located on three loci controlling resistance to CBD. The resistance varieties HDT and Catimor carry T locus [83], the moderate resistance variety K7 the recessive K gene, and the resistant variety Rume Sudan carries dominant R gene together with the recessive K gene. Later, Gichuru et al. [84] identified a locus that carried Ck-1 gene, localized within an 11 cM fragment, which was suggested to be synonymous to the T gene. They used 57 microsatellites and 31 AFLP markers; out of them, 8 AFLP and 2 microsatellites markers (Sat207 and Sat235) were closely linked to the resistance genotypes and were mapped to 1 chromosome fragment of C. canephora.

Further, Ck-1 gene was detected in all Ruiru 11 sibs using Sat235 [85]. Three to five recessive genes were reported to confer resistance to CBD in non-introgressed C. arabica by Ameha and Belachew [86]. Agwanda et al. [83] identified three RAPD markers, which were closely associated with CBD resistance using two susceptible cultivars (SL28 and Catura) and three resistant varieties (Rume Sudan, K7 and

Catimor). However, the use of RAPD markers was limited, due to their low reproducibility.

Studies on resistance mechanism of C. arabica to CBD revealed that antifungal compounds in the cuticle and on the wax from surface of green berries of resistant plants (Blue Mountain, Rume Sudan and SL 28) play an important role [49, 87–89]. These studies also showed that resistance could be related to the formation of cork barriers in both berries and hypocotyls [49, 81]. Biochemical and histological studies showed high increases in enzyme and peroxidase activity in susceptible plants compared to resistant ones [87], since in resistant plant the hyphal length inside the host tissues was significantly lower [90], while accumulation of phenolic compounds like flavonoids was increased [25, 26, 91–94]. Molecular studies [81, 95] identified various signaling pathways and defense response genes, as well as phytohormones involved in recognition and resistance to CBD.

Breeding for resistance to nematode

Although current control of nematode heavily relies on nematicides [64], the concern about environmental contamination and health around these toxic chemicals is increasing [96–98]. Furthermore, chemical control means additional expenses for the farmers (about 30% of field cost) [84], and difficulties with their application. Therefore, resistance breeding is an attractive strategy for controlling nematode populations [96, 98].

Resistant plants to nematodes can be obtained through either selection of breeding lines or screening germplasm, including related species and integration of resistance traits through conventional breeding methods, or engineered through molecular techniques [99, 100]. Some sources of resistance are controlled by a single dominant R gene, which may interact with the corresponding gene in the nematode. Noir et al. [101] identified a single gene, Mex-1, a partially dominant R gene, from the related coffee “IAPAR 59,” which reduces nematode (M. exigua) penetration, development, and subsequent galling [102].

So far, no nematode-resistant cultivar has been found in C. arabica. However, C. canephora and C. liberica var. dewevrei, Hong34, and Nhuantren were reported as natural hosts resistant to P. coffeae [103, 104]. Moreover, C. excelsa, Hong34, Nhuantren, and H1C19 were tolerant to R. arabocoffeae at the highest inoculation density (4000 nematodes/pot) [64, 105–107].

Previous studies have suggested that the presence of high levels of polyphenols in C. canephora roots suppresses the development of nematodes [108, 109]. Therefore, this variety could be used as a rootstock caring resistance/tolerance to P. coffeae and R. arabocoffeae, without any significant effect on the chemical composition of sugars, caffeine, trigonelline, chlorogenic acids, and lipids of coffee beans [103, 110, 111].

The C. canephora cv. Nemaya developed by hybridization of two C. canephora clones is resistant to P. coffeae and

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Meloidogyne spp. [111]. Furthermore, some resistance was identified in progenies of interspecific hybrid between C. arabica and C. canephora [66]. The genotypes Icatu H 4782/7/514 and Sarchimor C1669-33 showed poor resistance to brachyurus, although they are derived from an artificial hybrid between C. arabica and C. canephora with several backcrosses with C. arabica, and a cross between C. arabica cv. Vila Sarchi and the HDT CIFC 832/2, respectively [112].

Most of coffee resistant to Meloidogyne spp. (M. incognita, M. paranaensis, M. exigua, and M. arabicida) were found in accessions of C. canephora and its hybrids [65, 96, 97, 113, 114]. In 2003, a major resistance gene to M. exigua designated as Mex-1 was identified in C. canephora [101]. It was located in chromosome 3 harboring the SH3 gene [65]. It was reported that resistance to Meloidogyne spp. was involved in a hypersensitive-like response by interrupting the nematodes cycle after root penetration or during the migration and initial feeding steps [115, 116]. However, a highly virulent natural population of M. exigua broke the resistance in the cv. IAPAR 59 derived from hybrid containing Mex-1 resistance gene [116]. Alzipar et al. [102] concluded that Mex-1 might have an incomplete dominant expression. Histological analysis of roots of C. canephora “Clone 14,” highly resistant cultivar to both M. incognita races 1 and 3, showed late intense HR and root cell death. The death cells were found around young female nematodes and plant giant cells in response to nematodes infection [66].

Notwithstanding the abovementioned results, intensive research is required for effective management to control Meloidogyne spp. using resistant cultivars [117].

Natural source of resistance to diseases

Unfortunately, the vast majority of the world coffee production is based on two species, C. arabica and C. canephora. This results from low genetic diversity among coffee cultivars, which represents a massive limitation in the case of control and management of pest and disease under climatic changes.

In the case of narrow genetic diversity of coffee species, cross-breeding may be carried out to recover a desired and agronomically acceptable genetic background, hampered due to the long juvenile period of the tree crop. Consequently, coffee breeding is a resource- and time-consuming process lasting up to 30 years.

Most C. arabica cultivars are high yielding and produce a high-quality beverage, but are susceptible to pests and diseases, while most related diploid species such as C. canephora are resistant. Therefore, an interspecific transfer of resistance has become a priority in coffee breeding. A natural interspecific hybrid of C. arabica x·C. canephora raised Hibrido de Timor (HDT or Hybrid of Timor), showed resistance to various pathogens, such as coffee leaf rust (H. vastatrix), CBD (Colletotrichum kahawae), and root-knot nematodes (Meloidogyne spp). This natural

selection was the beginning of production of various introgressed lines in CIFC (HW26, Caturra Vermelho × HDT 832/1; H46, Caturra Vermelho × HDT 832/2; H361, Villa Sarchi × HDT 832/2; H528, Catuaí Amarelo × HW26/13), designated as Catimor and Sarchimor. After local selection, crosses with HDT produced IAPAR 59 (a cross between Villa Sarchi CIFC 971/10 and Hibrido de Timor CIFC 832/2) and dwarf IPR 107 (a cross between IAPAR 59 × Mundo Novo IAC3 376-4), Obata, Tupi and Oeiras in Brazil, Variedad Colombia (a cross between Hibrido de Timor 1343 and Caturra) in Colombia, Ihcafe-90 and Costa Rica 95 in Central America, Ihcafe-90 and Lempira (Honduras), Catisic (El Salvador) and Mida 96 (Panama) Riuru 11 in Kenya, and Sln 12 in India [29].

Furthermore, a breeding program for resistance to leaf-minor was carried out in Brazil by transferring resistance genes from C. racemosa to the susceptible C. arabica and producing a large number of hybrid progenies by using controlled crosses [100]. IPR 102, a cross between Catuai and Icatu, was developed at the IAC, and shown to be resistant to bacterial blight, and moderately resistant to rust [101].

Breeding programs can decrease crop losses by introducing diversity to existing cultivars, which can also improve the sustainability of coffee production worldwide by decreasing pest and disease and increasing yield and production. Therefore, to identify the individuals that can be integrated into a genetic improvement program, with the focus on morphological characteristics, yield, and resistance, required more studies on C. arabica in the center of origin (Ethiopia) [102]. Comprehensive information about the genetic bases of the resistance to biotic and abiotic stresses, plant architecture, yield, and other agronomical traits and improvement breeding in coffee is provided by various reports and reviews [16, 29, 51, 53,103–106].

Strategies for resistance for future breeding

Breeding for resistance to disease is an essential strategy for reducing crop yield losses. Selection for resistance can be improved by acquiring the knowledge of the evolution of coffee, existence of landraces and related species, availability of genetic diversity and genetic sources of resistance, establishment of breeding strategies and methods, as well as planting genotypes better suited and adapted to the cultivation areas. Crop yield losses vary between cultivars and regions; for example, in tropics and subtropical regions losses are higher since the conditions are favorable for disease development. Besides, it should be considered that breeding for resistance can be challenging since some pathogens can overcome resistance in established varieties. An example is the cultivar Oeiras MG 6851 (a cross between C. arabica cv. caturra (CIFC 19/1) and Hibrido de Timor (CIFC 832/1)), which was released as an important rust



resistant cultivar [107]. Twelve years later, the resistance was broken by race XXXIII of H. vastatrix [108]. An opposite example is given by two low-yielding C. arabica cultivars, Rume Sudan and Tafarikella, initially classified as susceptible, which in the field showed a considerable partial resistance [109].

Furthermore, screening for resistance and tolerance should be performed both at low and high initial inoculum densities. Some coffee accessions showed tolerance when initial inoculum densities were low but became susceptible at high initial inoculum densities. Therefore, for successful resistance breeding with a long-term effect, the dynamic, evolving nature of the host-pathogen interaction, level of genes, genotypes, populations, race specificity, biomolecules involved in plant defense, and adaptation to environmental conditions should be considered.

Breeding for resistance for multiple diseases

Some source of pathogens resistance is complex and is controlled by various genes of small effect [110]. There are minor genes, leading to progenies from crosses between resistant and susceptible lines, containing various phenotypes. Some source of resistance appears as single dominant R gene, known as a major gene. When pathogen contains a specific avirulence gene (Avr-genes), the R proteins can recognize any protein changes caused by a pathogen effector, which results in hypersensitive response (HR) [111]. In the absence of R genes, the plant target for the pathogen effector is not guarded, and therefore the disease will occur [79]. Considering, a single R gene is very often non-durable, mainly if it targets an effector that is not conserved, in the so-called pyramiding approach, multiple R genes will be introduced into a single host genome through conventional breeding or transformation. However, new pathogen strains can overcome host defense strategy, which is known as breakdown of the resistance. Therefore, the durability of resistance is an essential aspect for resistance breeding.

Since one of the aims of breeding programs is to introduce varieties that are strong and durable against pathogen and disease, these varieties should contain various resistance genes (polygenic and monogenic locus) that have low effect on the trait of interest.

Mutation breeding

Mutation induction has proven to be useful in the development of improved tree crop species characterized by self-compatibility, compact growth, and diseases resistance. Notable examples of disease-resistant mutants in woody/tree plants include Japanese pear, “Gold-Nijisseiki,” “Osa-Gold,” and “Kotobuki-Shinsui” with resistance to black spot disease [93, 94].

Among various mutation-induction techniques, physical mutagenesis with the use of X-ray radiation was the first

methodology that the researchers used [130]. Later, gamma-ray radiation proved to be useful to induce point mutations, chromosomal rearrangements, and bigger changes such as insertions and deletions [131]. Subsequently, chemical mutagenesis was used to induce point mutations, resulting in a different set of mutant alleles with silent, missense, nonsense, and splice site effects [132, 133]. Among various chemical mutagens, ethyl methanesulfonate (EMS) is frequently used to induce random mutations into the genome of different tissues and organs.

Two types of plant materials can be used in mutagenesis of tree crops, particularly in coffee mutation breeding [93, 94]: 1) multicellular such as seed, in vivo and in vitro cuttings as well as entire plants and 2) single-cell systems including anther, somatic cell from detached leaf, petal and pedicel meristem (Fig. 4). Mutagenesis of multicellular systems generates plant chimeras; therefore, additional work needs to be carried out leading toward dissolution of chimeric sectors. This is usually done by sectioning and subculturing the propagule until single homohistont or solid (uniform) mutant lines are produced. Whereas with seeds, chimera dissolution is mainly done by advancing mutant lines for at least two generations. The long juvenile or long-life cycle of tree crops makes the choice or strategy of starting material like seed too fastidious. Moreover, with multicellular systems, like stem cuttings, at least three rounds of sectioning and culture after mutagenesis are recommended before screening for desired mutants. Chimeras may be avoided if single cells rather than multiple cell systems are targeted for mutation induction. Obvious targets are cells, which can be grown into individual plants. Gametic cells, micro-spores and megaspores, which normally produce pollen and ovules in sexual reproduction are favored as they carry half the genome and in the process of chromosome doubling homozygosity can be fixed, including recessive mutations.

Thus, biotechnologies, especially cell and tissue culture, provide efficient tools for the propagation of target materials, mutation induction, mutant population development and selection. So, tree crop, that is, coffee with developed methods when used in mutation strategy can accelerate the production of new cultivars.

So far, the susceptibility of various coffee explants (seed, in vivo cuttings, in vitro cell/shoot explants) to physical and chemical mutagens has been determined [116–122] and few mutant populations have been developed for the purpose of resistance breeding. Mutagenesis (chemical or physical) can create additional new genetic variability in traits where the natural variability is not sufficient [123]. Accordingly, FAO/IAEA Joint program, a collaborative research effort through the IAEA’s Coordinated Research Project (CRP) was initiated in 2014 in cooperation with South American FAO/IAEA Member States focusing on different aspects of technology development and application for increasing the resilience of coffee to fungal pathogens.

However, the most important and difficult step in mutation breeding strategy is to screen the entire mutant

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population. Traditionally, forward genetics is a popular method to identify a trait of interest in the mutated population. However, it requires significant time and effort to screen the phenotypes of interest. A reverse genetic technology like TILLING (Targeting Induced Local Lesions in Genomes) combines traditional mutagenesis with high-throughput mutation discovery, which could identify the effect of a point mutation in specific genes. TILLING allows screening the mutated line from the M2 population by using a mismatch-specific endonuclease, which can identify a mutation in a gene of interest in a pool of DNA [142, 143]. TILLING relies on polymerase chain reaction (PCR), and therefore, the availability of the sequence of the gene of interest is a prerequisite of successful mutant selection.

Significant efforts toward rapid identification and discovery of induced mutations have been developed and commercialized for SNP calling using whole genome sequencing (WGS), RNA sequencing (RNA Seq), exome capture sequencing (ECS), restriction site-associated DNA sequencing (RADSeq), genotyping by sequencing (GBS), and TILLING by sequencing [144–146].

Genomic tools

Identified SNPs are not only valuable for breeding programs but also facilitate marker-assisted selection (MAS), quantitative trait loci (QTL), genome-wide association

studies (GWAS), and genomic selection (GS). In crop plants, QTLs and GWAS have been applied to identify genomic region affecting resistant phenotypes. Mapping of identified QTLs controlling resistance traits encompasses candidate genes/loci related to resistance traits/phenotypes, which could be applied in gene modification and crop improvement. The selected QTLs can be directly used in MAS without previous knowledge of functionality of genes underlying the QTLs. QTLs contain high number of candidate genes and make the identification of true casual gene difficult. On the other hand, GWAS provide mapping with much higher resolution without providing a segregating population. With available phenotypic data, GWAS enable the estimation of the position and effect of QTLS/genes without the need of extensive field experiments. Also, GWAS facilitate the identification of candidate genes for validation by mutagenesis and/or transformation [128]. However, association mapping and breeding improvement in C. arabica are very critical. Since it is self-pollinated, it contains low genetic diversity, less genomic resources, and fewer DNA markers. Therefore, it is essential to identify the population with high genetic diversity (e.g., Ethiopian germplasm) for any improvement program for the trait of interest.

Genome selection (GS) allows breeders to select traits that are influenced by large numbers of small-effect alleles in a wide range of genotypes. GS uses a high-throughput genotyping platform to identify alleles at many loci among the genome and to predict breeding and genotypic values of individuals with the best allelic combinations that

Figure 4. Mutation breeding scheme for treatment of in vitro coffee. (1) Mature donor plants provide vegetative buds, flower buds, and leaves, while seeds may be established directly as in vitro seedlings. (2) Establishment of in vitro cell and tissue cultures. (3) Mutagenesis of explants and cell cultures followed by chimera dissolution in case of multicellular explants, while in the case of single-cell systems the process can continue via plant regeneration. (4) Screening for traits of interest that can be conducted either in in vitro conditions prior to mutant acclimatization or in vivo upon acclimatization of plants in greenhouse or open field. (5) Selected improved cultivars can be released as direct mutants or can be integrated in breeding programs.



have not been phenotyped. Using GS in the context of resistance breeding for perennial crops increases the efficiency of breeding programs by shortening the length of the breeding cycles [147]. Selection in this approach is performed for large numbers of progeny that are the only genotype, and their phenotype can be predicted, and multi-trait indices can be developed to simultaneously select, for example, disease resistance even in environments where the disease is not present. This approach has been successfully applied to some diseases in crops such as maize, Eucalyptus, populous, and cassava [133, 148]. Furthermore, the development of high-throughput phenotyping could facilitate breeding for complex traits such as resistance, by allowing the study of many aspects of the plant resistance response. Therefore, GWAS and GS are promising methods for promoting the efficiency of resistance breeding for perennial plants like coffee.

Genomic tools and large-scale sequencing can significantly speed up the process of genetic analysis and crop improvement. This provides valuable information to breeders to understand the structure and diversity of the genetic resources, which can be used as a raw material for the development of new cultivars. While genomic approaches can increase our understanding of genes that are involved in host resistance, the identification of genes and their pathways underlying resistance to pathogens can help us to understand their effect, pathogen specificity, their contributions to durability, and to design a durable resistance line [128]. Resistance genes could also have a direct or indirect effect on another important trait. Further, resistance to one pathogen can cause susceptibility to another. While metabolic analyses have the potential to identify compounds related to defense mechanism, they are also crucial for their effect on nutritional quality and flavor of crops. Various studies and reviews highlight molecular and chemical response of coffee to abiotic treatment, which can be used for identification of resistance to pest and pathogens [22, 49, 50, 78, 122, 123, 149, 150].

The release of a reference genome of C. canephora allowed significant progress for C. arabica genomic analysis [121, 151]. The availability and release of draft genome sequences of C. arabica ([124], https://worldcoffeeresearch.org/work/coffea-arabica-genome/, https://phytozome.jgi.doe.gov/pz/portal.html#!info?alias=Org_C arabica_er]) as well as the generation of various EST sequences and BAC libraries in C. arabica [22, 150, 152–156] helped to identify genes and their regulatory sequences responsible for desirable traits.

Comparison of the coffee chromosomal region with grapevine and tomato genomes showed a correspondence of a one-to-one, and one-to-three, respectively. The enriched GO annotations of C. canephora were divided into two functional groups: defense response and metabolic process. Among the defense response group, nucleotide-binding and disease resistance genes are the most abundant categories. It was also suggested that the resistance genes (R-genes) in coffee are tandemly duplicated and altered from the linked gene families.

Sant’Ana et al. [16] used the reference genome of C. canephora to identify candidate genes representing potential targets for improving beverage quality with lipids and di-terpenes composition among 107 C. arabica accessions originated from wild populations in Ethiopia, by incorporating molecular breeding techniques to the traditional programs. Verified SNPs associated with the trait of interest by GWAS may be helpful to develop MAS aiming to improve not only the biochemical quality but also the resistance of the coffee beans. In parallel, Tran et al. [124] attempted to identify genes controlling the caffeine content in 18 genotypes of C. arabica with extreme high or low caffeine content. They were able to detect 65 caffeine-associated SNPs, among which 11 SNPs were associated with genes encoding enzymes involved in the conversion of substrates, which participate in the caffeine biosynthesis pathways. This analysis described the complex genetic control of caffeine biosynthesis in coffee, which is important in plant defense mechanisms.

Genome editing

In this review, emphasis is given to plant genetic resources and the progress that has been made in breeding resistance to economically important diseases in coffee. However, coffee breeders and researchers should also put effort not only in the identification of markers linked to a specific trait but also gaining insight into the function of the involved genes.

In contrast to conventional breeding, taking at least 20 years to release a new cultivar, biotechnological methods like insertional mutation, gene editing, somatic embryogenesis, and micro-propagation provide potent tools for coffee improvement and can also speed up the selection process of a superior plant [157]. Different tools were developed for precise genome editing by inducing double-stranded DNA breaks (DSBs) with programmable nucleases and nickases like engineered homing endonucleases/meganucleases (EMNs), zinc finger nucleases (ZFNs), transcription activator-like effector nucleases (TALENs), and clustered regularly interspaced short palindromic repeat/CRISPR-associated nuclease (CRISPR/Cas) [158–162]. Gene editing (GE) and insertional mutation have the potential to modify the DNA sequence of a single gene or multiple genes and to build blocks, alter or disrupt their functions and regulatory machinery that underlie the trait of interest, for example, disease susceptibility [133, 159, 163, 164].

GE has been used for targeted disruption of several susceptibility loci. Both TALENs and CRISPR/Cas9 technology were used in wheat to edit homeoalleles of MLO, which encodes a susceptibility factor for powdery mildew [165]. Disruption of the eukaryotic initiation factor locus, which promotes susceptibility to several potyviruses, improved resistance to several viruses in cucumber [166] and Arabidopsis [167]. In rice, resistance to bacterial blight was achieved by TALEN-mediated disruption of a sucrose

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efflux transporter gene [168], and CRISP/Cas9-induced mutations in a rice ethylene responsive factor (ERF) gene; the mutated genes conferred resistance to blast [169, 170]. Furthermore, CRISPR-Cas9 technology has been designed for editing genes controlling traits of importance in apple and grape in order to increase resistance to fire blight disease and powdery mildew, respectively [171]. The targeted mutation of OsMPK5 improved rice disease resistance [172]. Mutation at the promoter region of OsSWEET14 and OsSWEET11 genes, responsible for susceptibility to the bacterial blight, enhanced resistance to bacterial blight in Arabidopsis, tobacco, sorghum, and rice [173]. Transgenic plants expressing Cas9 and single guide RNAs (sgRNAs) targeting geminivirus sequences have been used to confer resistance to a range of geminiviruses in Nicotiana benthamiana and A. thaliana [128, 174–176]. The flexibility of such approaches is very advantageous since new sgRNA constructs can be designed when a viral target sequence mutates.

Both, TALENs and ZFNs were used widely for precise GE. However, some disadvantages are associated with these methods based on protein-DNA interactions for targeting. The constructions of large recognition domains are very labor- and cost-intensive, and the rate of failure is relatively high, especially for ZFNs. The CRISPR/Cas system is a cost-effective, fast, and precise alternative to the previous gene editing tools [159, 177]. Moreover, CRISPR GE can accelerate breeding program by targeting genes without foreign DNA. In adittion, although transgene integrations is hemizygous, CRISPR editing at the target loci is biallelic. In self-incompatible or dioecious perennial woody trees, biparental hemizygous Cas9/sgRNA transformation and the biallelic-edited gene can be produced [178]. Taken together, genome engineering by editing genes serves as a potential strategy for R genes in plants with durable resistance and resilience against diseases.

Conclusion and perspective

Here, the emphasis was to give an overview of coffee genetic resources and molecular tools that are used to detect and increase genetic diversity and to facilitate the resistance breeding program in coffee.

Validation of identified molecular markers across different coffee genotypes and wild species has been used for identification of genetic background, determination of inheritance of disease and pest resistance, and identification of markers linked to specific traits, which are essential for future breeding strategies. Traditional MAS has been successfully applied into the breeding material to the introgressed trait of interest such as disease resistance [71]. Several examples exist where disease tolerance could be increased in crop plants using induced mutations [Mutant Varieties Batabase (MVD); http://mvd.iaes.org]. Therefore, focusing on the development of technology

packages to improve mutation induction and screening for resistance of coffee to biotic threats could give a chance of a highly effective approach in introduction of novel genetic variation in tetraploid and diploid coffee.

As mutation discovery technologies improve and large-scale sequencing becomes cheap, it is expected that fast mutation identification for traits of interest will become straightforward for many plant research communities.

Access to the published coffee genome sequence could allow researchers and breeders to make resistance breeding of coffee more efficient. As approaches such as CRISPR/Cas become routine, the genetic toolkit for coffee improvement will expand further. This will allow fundamental, new biological insights, and the improvement of plants such as coffee. Further, an integrative view of genomics, transcriptomics, proteomics, and metabolomics data will enable to get to the bottom of some important physiological and molecular mechanisms unique to coffee pathogen resistance.

Climate change is predicted to affect many of the currently cultivated areas, by decreasing coffee production and increasing exposure and vulnerability of coffee to pests and diseases [91]. Therefore, technological advances are needed to facilitate the development of a superior plant with durable climate resilience and resistance to pathogens and pests. Among these, agronomic management, cultivar selection affected by various diseases and pathogens, as well as modeling can help to identify the most vulnerable and/or well-suited areas, cultivars, or populations for future demand, and to estimate the theoretical aspects of yield losses, the spread of pathogens and resistance durability under climate changes [25, 91]. Thus, no single method is sufficient alone, and an integrated approach is required.

Acknowledgements

The authors would like to thank Dr. Marzban for reading the manuscript and adding his valuable comments.

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