Introduction
Faba bean (Vicia faba L.) seeds are a generous source of plant protein, with a global average protein concentration of 29% on a dry-weight basis (Feedipedia, 2018). It is one of the main sources of affordable protein for human consumption in developing countries (consumed as dry or canned), and for livestock feed in many developed countries. The fresh pods and seeds are widely used as a vegetable crop for fresh seed production. Like other legumes, it symbiotically fixes atmospheric nitrogen, thus improving the soil fertility. As a non-host of many cereal pathogens, faba bean is ideal as a break between grain crops in the rotation (Köpke and Nemecek, Reference Köpke and Nemecek2010). It has a mixed breeding system and is cross-pollinated at frequencies of 4–84%, with the value determined by the interaction between the plant genotype, its environment and the population of pollinators (Bond and Poulsen, Reference Bond, Poulsen and Hebblethwaite1983). Its interaction with many species of bee (Stoddard and Bond, Reference Stoddard and Bond1987) makes it suitable for growing in ecological focus areas (Bues et al., Reference Bues, Preissel, Reckling, Zander, Kuhlman, Topp, Watson, Lindström, Stoddard and Murphy-Bokern2013). It is widely adapted to cool-temperate agriculture, being grown from Mediterranean climates in southern Australia and Mediterranean basin countries to sub-boreal climates in Finland and Canada. Nevertheless, faba bean cultivation is limited due to its susceptibility to several biotic and abiotic constraints globally (see Stoddard et al., Reference Stoddard, Balko, Erskine, Khan, Link and Sarker2006; Torres et al., Reference Torres, Roman, Avila, Satovic, Rubiales, Sillero, Cubero and Moreno2006; Khan et al., Reference Khan, Paull, Siddique and Stoddard2010). Hence, genetically diverse sources of resistance genes or genes for specific adaptations such as to abiotic stress factors are required in pre-breeding programmes worldwide. Some of these germplasm sources, called ‘donors’, may become prominent.
Faba bean is represented in germplasm collections by only the cultivated form. Both botanical and molecular data suggest that the wild ancestors of faba bean either have vanished or have not yet been discovered (Maxted, Reference Maxted1993; Duc et al., Reference Duc, Bao, Baum, Redden, Sadiki, Suso, Vishniakova and Zong2010; Kosterin, Reference Kosterin2014; Caracuta et al., Reference Caracuta, Weinstein-Evron, Kaufman, Yeshurun, Silvent and Boaretto2016), which highlights the importance of the accessible diversity within the cultivated form. The place of origin of faba bean is still unknown. A Near or Middle East centre of origin has been proposed (Cubero, Reference Cubero1974), and the earliest identified remains of faba bean date from 10,200 BP in a cave in Israel (Caracuta et al., Reference Caracuta, Barzilai, Khalaily, Milevski, Paz, Vardi, Regev and Boaretto2015). Radiation followed in four directions from the proposed centre: Europe, along the North Africa coast to Spain, along the Nile Valley to Ethiopia and from Mesopotamia to India and China (Lawes et al., Reference Lawes, Bond, Poulsen and Hebblethwaite1983). Spanish and European material was taken to South America in the 16th century (Bond, Reference Bond and Simmonds NW1976). There are 43,695 faba bean accessions conserved within 37 global genebanks (ex situ, FAO, 2010) as well as on-farm conservation (in situ, Kumar et al., Reference Kumar, Singh, Elanchezhian, Sundaram, Singh and Bhatt2012). ICARDA (International Center for Agricultural Research in the Dry Areas) hosts the largest collection of over 9500 accessions (21% of global collection, FAO, 2010). ICARDA maintains its faba bean germplasm in two classes, international legume bean (ILB) accessions from different countries, and bean pure line (BPL) accessions that are derived through selfing from accessions drawn from the ILB collection (Saxena and Varma, Reference Saxena and Varma1985).
Accession ILB 938
ILB 938 is the result of mass selection from ILB 438 based on seed size. ILB 438 was brought to ICARDA from the Andean region of Ecuador and Columbia (Robertson, Reference Robertson, Chapman and Tarawali1984) in 1973. ICARDA's registered BPL derivatives of ILB 438 and ILB 938 are BPL 710 and BPL 1179, respectively. ILB 938/2 is an inbred line developed at Göttingen for use in genetics and breeding studies. The corresponding ‘IG’ number for ILB 938 in the ICARDA genebank is ‘IG 12132’ (accession doi: 10.18730/60FD2, see https://www.genesys-pgr.org/10.18730/60FD2). ILB 438 is registered as IG 11632 in the ICARDA genebank (accession doi: 10.18730/601TB).
Morphological markers
In the wild-type faba bean, the extra-floral nectary on the stipule is coloured black. The presence of stipule-spot pigmentation was proposed as an early morphological marker indicating wild-type ‘coloured’ flowers (tannin-containing faba bean), where there is a black spot on each wing petal and dark vein markings on the standard petal (Picard, Reference Picard1976). The absence of the pigmentation was considered as the corresponding early morphological indicator for the white-flower, zero-tannin trait (Link et al., Reference Link, Hanafy, Malenica, Jacobsen, Jelenić, Kole and Hall2008). ILB 938, however, carries a rare allele (ssp1) that decouples pigmentation in flowers from that in stipules, so it has colourless stipules and coloured flowers (online Supplementary Fig. S1, Khazaei et al., Reference Khazaei, O'Sullivan, Sillanpää and Stoddard2014a). An Australian line, AF11212, has the same phenotype and is derived from BPL 710 (Dr Jeff Paull, The University of Adelaide, Australia; personal communication). Crossing ILB 938/2 with AF11212 (including reciprocal crosses) showed in the F1 and F2 generations uniformly the combination of colourless stipule spots and spotted flowers, confirming that the same gene exists in both accessions (Miller, Reference Miller2016).
The seed size of ILB 938 is classified as equina (horse bean, field bean, flattened seed; 0.6 g/seed), which is expected since it was the medium- to large-seeded Mediterranean-adapted faba bean form that was introduced to Central and South America by immigrants from Spain (Muratova, Reference Muratova1931; Cubero, Reference Cubero1974). The seed coat of ILB 938 is green in colour, which is recessive to the common beige or buff colour (Khazaei et al., Reference Khazaei, O'Sullivan, Sillanpää and Stoddard2014b).
A further noticeable morphological character of ILB 938 is the clinging pod wall, where fibres from the inner epidermis of the pod cling to the surface of the seed (online Supplementary Fig. S2). We have not seen this trait otherwise reported in faba bean germplasm, and while it is of little importance agronomically or economically, it may indicate a difference in cell wall development that has other impacts elsewhere in the plant or in the value chain.
Finally, the funiculus is yellow in ILB 938, in contrast to the common green displayed by other accessions.
Biotic stresses
The resistance of ILB 938 to chocolate spot (CS, caused by Botrytis fabae Speg.) has been demonstrated in Egypt (Mohamed et al., Reference Mohamed, Zeid and Habib1981 [re-coded NEB 938]; Khalil and Nassib, Reference Khalil and Nassib1984; Robertson, Reference Robertson, Chapman and Tarawali1984), Syria (Hanounik, Reference Hanounik1982), the UK (Jellis et al., Reference Jellis, Bond and Old1982), Canada (Robertson, Reference Robertson, Chapman and Tarawali1984), France (Tivoli et al., Reference Tivoli, Berthelem, Leguen and Onfroy1988), and Ethiopia (Beyene et al., Reference Beyene, John, Sibiya and Fikre2016). Further, we have noticed its resistance to CS in field conditions of both southern Finland and western Canada.
The resistance of the original source of ILB 938 was confirmed in the Nile Delta after crosses with the local cultivar Giza 3 (ICARDA Caravan, 1998; Zeid et al., Reference Zeid, Mitchell, Link, Carter, Nawar, Fulton and Kresovich2009). From there, it was transferred to locally adapted material that was released as Giza 461 in Egypt (Bond et al., Reference Bond, Jellis, Rowland, Le Guen, Robertson, Khalil and Li-Juan1994; Dwivedi et al., Reference Dwivedi, Blair, Upadhyaya, Serraj, Balaji, Buhariwalla, Ortiz and Crouch2006; El-Komy et al., Reference El-Komy, Saleh and Molan2015).
The related BPLs BPL 710 and BPL 1179 to ILB 438 and ILB 938, respectively, also showed high resistance to CS across environments (Hanounik and Maliha, Reference Hanounik and Maliha1986; Hanounik and Robertson, Reference Hanounik and Robertson1988; Villegas-Fernández et al., Reference Villegas-Fernández, Sillero and Rubiales2012; Beyene et al., Reference Beyene, Derera and Sibiya2018). The Australian cultivar Icarus was derived from BPL 710 and released as a cultivar resistant to CS and rust (Dwivedi et al., Reference Dwivedi, Blair, Upadhyaya, Serraj, Balaji, Buhariwalla, Ortiz and Crouch2006).
ILB 938 is, furthermore, considered as a consistent source of resistance to rust (Uromyces viciae-fabae (Pers.) J. Schrot.) (Khalil et al., Reference Khalil, Nassib and Mohammed1985; Rashid and Bernier, Reference Rashid and Bernier1986; Rashid and Bernier, Reference Rashid and Bernier1991). Both BPL 710 (Australian accession No. AC1269) and BPL 1179 (AC1272) are registered as rust-resistant accessions in Australia (Ijaz et al., Reference Ijaz, Adhikari, Stoddard and Trethowan2018) as well as in ICARDA (1987).
Some studies have suggested that ILB 938 may also carry resistance to crenate broomrape, Orobanche crenata Forsk., an achlorophyllous, holoparasitic weed, poses a major constraint to faba bean production in Mediterranean climates (Zeid et al., Reference Zeid, Ghazy and Link2006, Reference Zeid, Mitchell, Link, Carter, Nawar, Fulton and Kresovich2009).
Abiotic stresses
Drought adaptation is an essential character for faba bean cultivation in arid and semiarid regions. ILB 938 has demonstrated high water use efficiency (WUE) in several studies (e.g. Abdelmula et al., Reference Abdelmula, Link, von Kittlitz and Stelling1999; Link et al., Reference Link, Abdelmula, von Kittlitz, Bruns, Riemer and Stelling1999; Stoddard et al., Reference Stoddard, Balko, Erskine, Khan, Link and Sarker2006; Khan et al., Reference Khan, Link, Hocking and Stoddard2007, Reference Khan, Paull, Siddique and Stoddard2010; Khazaei et al., Reference Khazaei, Street, Bari, Santanen and Stoddard2013; Khazaei et al., Reference Khazaei, O'Sullivan, Sillanpää and Stoddard2014b) mainly due to low stomatal conductance, thus minimizing water loss and maintaining yield under drought conditions. Nevertheless, its reduced leaf stomatal conductance was not associated with a highly ramified rooting system (Belachew et al., Reference Belachew, Nagel, Fiorani and Stoddard2018).
While ILB 938 has relatively low productivity, no yield penalty was observed when it was exposed to drought conditions (Link et al., Reference Link, Abdelmula, von Kittlitz, Bruns, Riemer and Stelling1999; Khan et al., Reference Khan, Link, Hocking and Stoddard2007; Khazaei et al., Reference Khazaei, O'Sullivan, Sillanpää and Stoddard2014b). It maintains a relatively high water status under water-deficit conditions, demonstrating high WUE with relatively low yield, because its stomata shut early, reducing potential photosynthesis while limiting water loss.
The response of ILB 938/2 to ultraviolet light differs greatly from that of a contrasting cultivar, Aurora/2 that was developed at low altitudes and high latitudes where incident UV is much weaker than high in the Andes (Yan et al., Reference Yan, Neugart, Stoddard and Aphalo2018).
Mapping populations
A population of recombinant inbred lines (RILs) was developed from the cross of Mélodie/2 × ILB 938/2 (along with its reciprocal) at the University of Helsinki (Khazaei et al., Reference Khazaei, O'Sullivan, Sillanpää and Stoddard2014a). This population has been mapped for traits related to drought adaptation (Khazaei et al., Reference Khazaei, O'Sullivan, Sillanpää and Stoddard2014b), vicine–convicine concentration (v–c, Khazaei et al., Reference Khazaei, O'Sullivan, Jones, Pitts, Sillanpää, Pärssinen, Manninen and Stoddard2015) and stipule-spot pigmentation (Khazaei et al., Reference Khazaei, O'Sullivan, Sillanpää and Stoddard2014a). Quantitative traits loci for seed size, seed coat colour, clinging pod wall and yellow funiculus have also been located. ILB 938 and Mélodie differed at two loci affecting stomatal activity at opposite ends of chromosome II, with each parent contributing a canopy-cooling allele (Khazaei et al., Reference Khazaei, O'Sullivan, Sillanpää and Stoddard2014b). The progenies of this population facilitated the development of a reliable molecular marker for v–c in this crop (Khazaei et al., Reference Khazaei, Purves, Song, Stonehouse, Bett, Stoddard and Vandenberg2017). This population is being phenotyped for salinity response in a collaboration with Egypt, and collaborative studies on other traits are in progress. Near-isogenic lines have been derived from heterozygous F5 individuals at Göttingen (Tacke and Link, Reference Tacke and Link2017).
Another RIL population, ILB 938/2 × Disco/2 (Khazaei et al., Reference Khazaei, O'Sullivan, Sillanpää and Stoddard2014a), is suitable for CS genetic studies. Disco (low in both tannin and v–c) has been shown to be very sensitive to CS (Villegas-Fernández et al., Reference Villegas-Fernández, Sillero and Rubiales2012; Khazaei, Personal observation). An RIL population from ILB 938/2 × Aurora/2 (Khazaei et al., Reference Khazaei, O'Sullivan, Sillanpää and Stoddard2014a) will be useful for analysing the basis of the difference in ultraviolet response of these two lines.
A multi-parent population [(Disco/2 × ILB 938/2) × (IG 114476 × IG 132238)] has been prepared for use in genomic studies (Khazaei et al., Reference Khazaei, Stoddard, Purves and Vandenberg2018). This population is at F4 generation at the time of writing this paper and kept at the University of Reading, UK.
DNA fingerprinting
ILB 938/2 was genotyped using 875 single nucleotide polymorphism markers developed by Webb et al. (Reference Webb, Cottage, Wood, Khamassi, Hobbs, Gostkiewicz, White, Khazaei, Ali, Street, Stoddard, Maalouf, Ogbonnaya, Link, Thomas and O'Sullivan2016). The results showed a high level of homozygosity (99.6%, Webb et al., Reference Webb, Cottage, Wood, Khamassi, Hobbs, Gostkiewicz, White, Khazaei, Ali, Street, Stoddard, Maalouf, Ogbonnaya, Link, Thomas and O'Sullivan2016). The genotyping calls on ILB 938/2 are presented in online Supplementary Table S1.
Conclusions
The presence of unusual traits in this material is intriguing, because the crop has been grown in South America for only about 500 of its 10,000 years of domestication. It may be attributable to several causes, including widespread genetic variation introduced by the European settlers, adaptation to extremely varied environments within short distances due to altitude, frequent gene exchanges by pollinators and movement of peoples, and natural selection (Bond et al., Reference Bond, Jellis, Rowland, Le Guen, Robertson, Khalil and Li-Juan1994), or UV-induced mutation. Recently, several new accessions from Spain, Ecuador, Colombia and Peru with high level of resistance to CS were identified (Maalouf et al., Reference Maalouf, Ahmed, Shaaban, Bassam, Nawar, Singh and Amri2016).
Supplementary material
The supplementary material for this article can be found at https://doi.org/10.1017/S1479262118000205.
Acknowledgements
The authors thank Dr Jeff Paull (The University of Adelaide, Australia) for providing the seeds of AF11212. ILB 938 (IG 12132) is also acknowledged for its generous offering. FLS dedicates this paper to the memory of faba bean breeder extraordinaire Dr David Bond (1929–2017), who was a kind mentor and teacher.
