Fabaceae — Systematics of Legumes

1.1. Taxonomic Status and Scope of the Family

The legume family (Fabaceae, or Leguminosae) occupies third place among all families of flowering plants in number of species, yielding only to Asteraceae (composites) and Orchidaceae (orchids) (LPWG, 2017; Judd et al., 2018). According to modern estimates, the family includes about 770 genera and more than 19,500 species (LPWG, 2017). For comparison: the family Poaceae (grasses) contains about 12,000 species, and Rosaceae (roses) about 3,000 species (Judd et al., 2018). Thus, legumes represent one of the largest and most diverse groups of land plants.

The name of the family — Fabaceae — derives from the type genus Faba Mill. (= Vicia L.), but the alternative name Leguminosae is also widely used in the literature; it has priority in some classification systems (Lewis & Schrire, 2003; LPWG, 2017). Both names are recognized by the International Code of Nomenclature for algae, fungi, and plants (Melbourne Code) as interchangeable (McNeill et al., 2012; LPWG, 2017).

1.2. Geographic Distribution and Ecological Amplitude

Legumes are a cosmopolitan group, occurring on all continents except Antarctica, and in almost all biomes — from Arctic tundras to tropical rainforests, from deserts to wetlands (Schrire et al., 2005a, b; LPWG, 2017). They are significant ecological components of almost all terrestrial ecosystems: they dominate in dry tropical forests and savannas, play an important role in Mediterranean, desert, and temperate communities, and reach high latitudes and elevations (LPWG, 2017).

The ecological amplitude of legumes is striking. Among them are:

• Large emergent tropical trees with buttress roots (for example, some species of Inga, Parkia);
• Shrubs and subshrubs of deserts and savannas (Acacia s.l., Prosopis);
• Herbaceous annuals and perennials of temperate latitudes (Pisum, Vicia, Trifolium, Medicago);
• Lianas and climbers with or without tendrils (Lathyrus, Vigna, Mucuna);
• Epiphytes and succulents (some tropical representatives);
• Aquatic plants (rarely, for example, Neptunia oleracea);
• Geoxylic subshrubs with woody underground organs (LPWG, 2017).

Such diversity of life forms and ecological strategies makes legumes one of the most successful groups of flowering plants.

1.3. Importance in Human Nutrition

Legumes play an exceptional role in human nutrition. In economic importance, the family is second only to Poaceae (grasses) (LPWG, 2017). The main food products obtained from legumes can be divided into several categories:

Grain legumes (pulses) are legumes grown for dry seeds. They are the most important source of plant protein: seeds contain from 20 to 25% protein, as well as carbohydrates, fiber, vitamins, and minerals (Rubatzky & Yamaguchi, 1997; Prohens & Nuez, 2008). Among the most important grain legumes:

• Pea (Pisum sativum) — one of the oldest crops of the Old World, cultivated for more than 7000 years (Rubatzky & Yamaguchi, 1997);
• Lentil (Lens culinaris) — an important source of protein in the Mediterranean, South Asia, and the Middle East (Rubatzky & Yamaguchi, 1997);
• Chickpea (Cicer arietinum) — the second most important grain legume in the world after soybean, the main source of protein in India and South Asian countries (Rubatzky & Yamaguchi, 1997);
• Common bean (Phaseolus vulgaris) — a crop of American origin, now distributed worldwide; includes both dry and vegetable (snap) forms (Prohens & Nuez, 2008; Rubatzky & Yamaguchi, 1997);
• Soybean (Glycine max) — the most important oil and protein crop of East Asian origin; seeds contain up to 50% protein and up to 25% oil (Rubatzky & Yamaguchi, 1997);
• Peanut (Arachis hypogaea) — a crop of American origin, cultivated for seeds rich in protein (about 30%) and oil (up to 50%) (Rubatzky & Yamaguchi, 1997);
• Vigna (Vigna spp.) — includes mung bean (V. radiata), urd (V. mungo), cowpea (V. unguiculata), and other important crops of the tropics and subtropics (Rubatzky & Yamaguchi, 1997);
• Pigeon pea (Cajanus cajan) — an important crop of dry tropics, especially in India and East Africa (Rubatzky & Yamaguchi, 1997).

Vegetable legumes are crops in which immature pods, immature seeds, or young shoots are used as food. These include:

• Snap bean (Phaseolus vulgaris) — immature pods consumed fresh, frozen, or canned (Nonnecke, 1989; Rubatzky & Yamaguchi, 1997);
• Green pea (Pisum sativum) — immature seeds widely used fresh and canned (Rubatzky & Yamaguchi, 1997);
• Sugar pea (Pisum sativum var. macrocarpum) — immature pods consumed whole (Rubatzky & Yamaguchi, 1997);
• Broad bean (Vicia faba) — large-seeded forms used as a vegetable crop (Rubatzky & Yamaguchi, 1997);
• Lima bean (Phaseolus lunatus) — a crop of American origin, used both fresh and dry (Rubatzky & Yamaguchi, 1997);
• Yardlong bean (Vigna unguiculata cultigroup sesquipedalis) — a popular vegetable crop of Southeast Asia (Rubatzky & Yamaguchi, 1997).

Other food products — legumes also provide:

• Soybean oil — one of the most important vegetable oils in the world (Rubatzky & Yamaguchi, 1997);
• Peanut oil — a food product obtained from peanut seeds (Rubatzky & Yamaguchi, 1997);
• Soy sauce, tofu, miso — products of soybean fermentation, traditional in East Asia (Rubatzky & Yamaguchi, 1997);
• Mung bean sprouts — a popular product in Asian cuisine (Rubatzky & Yamaguchi, 1997);
• Tamarind (Tamarindus indica) — a spice and food product (LPWG, 2017);
• Carob (Ceratonia siliqua) — fruits used as a chocolate substitute and livestock feed (LPWG, 2017).

The nutritional value of legumes is exceptionally high. They are rich in protein, fiber, vitamins (especially B vitamins), minerals (iron, calcium, magnesium, zinc), and contain little fat (Rubatzky & Yamaguchi, 1997; Prohens & Nuez, 2008). Legume proteins are often limited in sulfur-containing amino acids (methionine and cysteine), but when combined with cereals, which are rich in these amino acids but poor in lysine, a complete amino acid profile is achieved (Rubatzky & Yamaguchi, 1997). It is this combination — cereals + legumes — that underlies the traditional diets of many peoples of the world.

1.4. Importance in Animal Feed

Legumes play a key role in feed production. They are used as:

• Forage grasses — alfalfa (Medicago sativa), clover (Trifolium spp.), sainfoin (Onobrychis spp.), vetch (Vicia spp.), sweet clover (Melilotus spp.) (Rubatzky & Yamaguchi, 1997; LPWG, 2017);
• Silage crops — maize + soybean, sorghum + cowpea, and other mixtures (Connor et al., 2011);
• Green feed — fresh green mass fed to livestock (Connor et al., 2011);
• Hay and haylage — conserved feeds from legume grasses (Connor et al., 2011);
• Concentrated feeds — seeds of soybean, pea, lupine used in the feed industry (Rubatzky & Yamaguchi, 1997).

Legume feeds are characterized by high protein content (15–25% in dry matter), good digestibility, and nutritive value (Connor et al., 2011). Alfalfa, clover, and other legume grasses are the basis of pasture and hay feed production in many regions of the world. For example, in Europe and North America, alfalfa and clover occupy millions of hectares and provide high-quality feed for dairy and beef cattle (Connor et al., 2011).

1.5. Role in Crop Rotation and Nitrogen Accumulation in Soil

One of the most important features of legumes is their ability for symbiotic nitrogen fixation — a process in which atmospheric molecular nitrogen (N₂) is converted into forms available to plants (ammonia, amino acids) with the help of rhizobia bacteria living in nodules on roots (Marschner, 2012; Lambers & Oliveira, 2019). This process makes legumes unique among agricultural crops, since they not only satisfy their own nitrogen needs but also enrich the soil with nitrogen available to subsequent crops.

The contribution of legumes to the nitrogen balance of agrocenoses is enormous. According to estimates, biological nitrogen fixation provides from 40 to 70 million tons of nitrogen per year globally (Herridge et al., 2008; Marschner, 2012). Symbiotic nitrogen fixation by legumes accounts for about 50% of this amount. Depending on the species, growing conditions, and rhizobial efficiency, legumes can fix from 25 to 250 kg of nitrogen per hectare per season, and under favorable conditions up to 500 kg N/ha per year (Marschner, 2012). For example:

• Alfalfa (Medicago sativa) — 180–780 kg N/ha per season (Marschner, 2012);
• Clover (Trifolium spp.) — 64–250 kg N/ha (Marschner, 2012);
• Soybean (Glycine max) — 15–250 kg N/ha (Marschner, 2012);
• Pea (Pisum sativum) — 86 kg N/ha (Marschner, 2012);
• Lupine (Lupinus spp.) — 150–170 kg N/ha (Marschner, 2012).

Including legumes in crop rotations is one of the cornerstones of sustainable agriculture. Legume predecessors increase the yield of subsequent crops by 30–35% compared with cereal monoculture (Khan et al., 2019). For example, maize after soybean or alfalfa requires 40–50 kg N/ha less nitrogen fertilizer (Connor et al., 2011). This not only reduces fertilizer costs but also reduces environmental pollution associated with the production and application of nitrogen fertilizers (greenhouse gases, nitrate leaching into groundwater, eutrophication of water bodies) (Connor et al., 2011; Marschner, 2012).

Legumes are also used as green manure crops — plants grown specifically to be plowed into the soil to enrich it with organic matter and nitrogen (Connor et al., 2011). Classic green manures are lupine, vetch, sweet clover, clover, and serradella (Ornithopus sativus). Green manuring improves soil structure, increases organic matter content, suppresses weeds, and reduces erosion (Connor et al., 2011).

1.6. Diversity of Life Forms

As already noted, legumes demonstrate exceptional diversity of life forms (LPWG, 2017; Judd et al., 2018):

Trees. Many tropical legumes are large trees forming the forest canopy. For example, species of Parkia, Inga, Dipteryx, Pterocarpus, Dalbergia reach heights of 30–40 m and more. Some legumes are emergents rising above the main canopy of the tropical forest. The wood of many legumes (for example, Dalbergia, Pterocarpus, Intsia) belongs to the category of valuable timbers and is used for furniture, musical instruments, and parquet (LPWG, 2017).

Shrubs. Many legumes are shrubs dominating savannas, Mediterranean maquis, deserts, and semi-deserts. For example, species of Acacia s.l., Prosopis, Calliandra, Senna form shrub thickets in arid and semi-arid regions (LPWG, 2017).

Herbs. Herbaceous legumes are the most important component of meadows, steppes, prairies, and pastures of temperate and subtropical latitudes. These include Trifolium, Medicago, Lotus, Vicia, Lathyrus, Astragalus (the largest genus of the family — about 2000 species) (LPWG, 2017; Judd et al., 2018).

Lianas. Many tropical legumes are lianas climbing tree trunks with tendrils (for example, Lathyrus, Vicia) or twining around support (Mucuna, Vigna, Dolichos). Some lianas reach lengths of 50 m and more (LPWG, 2017).

Aquatic plants. Few legumes are adapted to the aquatic environment. For example, Neptunia oleracea is a floating aquatic plant of the tropics; Aeschynomene spp. can grow on waterlogged soils (LPWG, 2017).

Succulents and xerophytes. Some legumes are adapted to extremely dry conditions. For example, Prosopis spp. (mesquite) are deep-rooted shrubs and trees of the deserts of North America and the Middle East; Acacia spp. of Australian deserts are xerophytic shrubs with phyllodes (LPWG, 2017).

Such diversity of life forms reflects the broad ecological plasticity of the family and its ability to adapt to the most varied environmental conditions.

1.7. Economic Importance: General Overview

Besides food and feed importance, legumes are used by humans for many other purposes (LPWG, 2017):

• Wood — Dalbergia (rosewood, palisander), Pterocarpus (padauk), Intsia (merbau), Acacia (acacia), Prosopis (mesquite) — valuable timbers for furniture, construction, musical instruments;
• Tannins — Acacia spp. (acacia), Caesalpinia spp. — sources of tannins for the leather industry;
• Gums and resins — Acacia senegal (gum arabic), Astragalus spp. (tragacanth), Hymenaea (copal) — used in food, pharmaceutical, and textile industries;
• Dyes — Indigofera (indigo), Haematoxylum (logwood), Caesalpinia (brasilin) — sources of natural dyes;
• Medicinal plants — Glycyrrhiza (licorice), Astragalus (astragalus), Sophora (sophora), Erythrina (erythrina), Piscidia (fish poison root) — sources of biologically active compounds;
• Ornamental plants — Robinia (black locust), Wisteria (wisteria), Lupinus (lupine), Delonix (flamboyant), Bauhinia (bauhinia), Acacia (acacia) — widely cultivated in gardens and parks;
• Insecticides — Derris (derris), Lonchocarpus (lonchocarpus) — sources of rotenone;
• Tanning substances — Acacia, Caesalpinia, Prosopis — sources of tannins;
• Essential oils — Acacia (acacia), Dipteryx (tonka), Myroxylon (Peru balsam) — used in perfumery.

Thus, legumes are not only the most important food and feed crops but also sources of many industrial products, medicines, and ornamental plants.

2.1. Place of Fabaceae in the System of Flowering Plants

The family Fabaceae (Leguminosae) belongs to the order Fabales — one of the best-defined orders in the system of flowering plants (Judd et al., 2018). The order Fabales includes four families: Fabaceae, Polygalaceae (milkworts), Surianaceae, and Quillajaceae (LPWG, 2017; Judd et al., 2018). The monophyly of the order Fabales is reliably confirmed both by molecular phylogenetic data (analysis of plastid and nuclear gene sequences) and by morphological synapomorphies: simple vessel perforations, clawed petals, large green embryo (Judd et al., 2018; LPWG, 2017).

Phylogenetic relationships within the order Fabales are as follows (Judd et al., 2018):

• Polygalaceae — sister group to the clade uniting the remaining three families;
• Surianaceae and Quillajaceae — successively sister groups to Fabaceae;
• Fabaceae — the largest and most specialized family of the order, sister to the clade Surianaceae + Quillajaceae.

Thus, the closest relatives of legumes among modern flowering plants are the small families Surianaceae (shrubs and trees of the tropics and subtropics) and Quillajaceae (one family with one genus Quillaja, growing in South America) (Judd et al., 2018). Together they form a well-supported clade within the order Fabales.

The order Fabales, in turn, belongs to the fabid clade (Fabidae, eurosids I) within the group rosids (Rosidae), which together with malvids (Malvidae) forms the clade superrosids (Superrosidae) within eudicots (Eudicotyledoneae) (Judd et al., 2018; LPWG, 2017). Such a phylogenetic position means that legumes are evolutionarily related to such economically important families as Rosaceae (roses), Fagaceae (beeches), Betulaceae (birches), Cucurbitaceae (cucurbits), as well as to the orders Malpighiales, Sapindales, and others (Judd et al., 2018).

2.2. Monophyly of the Family Fabaceae

The monophyly of the family Fabaceae (Leguminosae) is beyond doubt and is confirmed by both molecular and morphological data (LPWG, 2017; Judd et al., 2018). Among the key morphological synapomorphies of the family, the following should be mentioned (Judd et al., 2018; LPWG, 2017):

1. Gynoecium of one carpel (monocarpous gynoecium) with a superior ovary, one locule, marginal placentation, and usually two or many ovules arranged in two rows on one placenta. This is the most striking and universal characteristic of the family; only in rare cases (for example, in some representatives of the genus Inga) is a multicarpellary gynoecium observed (LPWG, 2017).

2. Fruit — a legume — a dry, usually longitudinally dehiscent fruit formed by one carpel. The legume may be many-seeded or one-seeded, dehiscent or indehiscent, dry or fleshy, winged or wingless (Judd et al., 2018; Rubatzky & Yamaguchi, 1997). It is this fruit type that gave the name to the entire family.

3. Flowers usually bisexual, with a calyx of 5 (rarely 4 or 6) sepals, usually fused, and a corolla of 5 (rarely 4 or 6) petals, usually free or partially fused. Stamens usually 10, rarely 5, 4, or numerous; they often fuse into a tube (monadelphous) or into two groups (diadelphous) (Judd et al., 2018; LPWG, 2017).

4. Leaves usually compound, pinnate, bipinnate, trifoliate, or palmate, with well-developed pulvini at the base of the leaf and leaflets, with stipules (Judd et al., 2018; Rubatzky & Yamaguchi, 1997). Pulvini provide the so-called “sleep movements” of leaves and are a characteristic feature of many legumes.

5. Symbiosis with nitrogen-fixing bacteria (rhizobia) with the formation of root nodules — although this is not a universal characteristic (not all legumes form nodules), it is widespread and has enormous ecological and agronomic importance (Marschner, 2012; Lambers & Oliveira, 2019). We will discuss this in more detail in Chapter 4.

6. Specific chemical composition: frequent presence of alkaloids, tannins, flavonoids, non-protein amino acids (for example, canavanine), cyanogenic glycosides; in many legumes, storage proteins accumulate in seeds — leghemoglobin and globulins (legumin, vicilin) (Judd et al., 2018; LPWG, 2017).

It should be emphasized that, despite enormous morphological diversity, all legumes are united by a common plan of flower and fruit structure, which makes the family easily recognizable even to a non-specialist.

2.3. Traditional Division of the Family into Three Subfamilies

For more than 140 years, beginning with the classical work of Bentham (1865) and until the end of the 20th century, the family Fabaceae was traditionally divided into three subfamilies (Polhill et al., 1981; Lewis et al., 2005; Sharma, 2009):

1. Faboideae (or Papilionoideae) — papilionoid legumes;

2. Mimosoideae — mimosa legumes;

3. Caesalpinioideae — caesalpinioid legumes.

This division was based mainly on floral characters, primarily on the type of aestivation (arrangement) of petals in the bud and flower symmetry (LPWG, 2017; Judd et al., 2018):

• Faboideae (Papilionoideae) — flowers usually zygomorphic, papilionaceous: the upper (adaxial) petal — the “standard” (vexillum, standard) — is the largest and is positioned outside (outermost); two lateral petals — “wings” (alae, wings) — and two lower petals, often fused into a “keel” (carina, keel). This arrangement is called descending imbricate aestivation (Judd et al., 2018).

• Mimosoideae — flowers usually actinomorphic (radially symmetrical), small, gathered in dense capitate or spicate inflorescences; petals in the bud valvate — that is, they do not overlap by edges but are closed by valves (Judd et al., 2018; LPWG, 2017).

• Caesalpinioideae — flowers usually zygomorphic, but not papilionaceous; the upper (adaxial) petal is usually the innermost (positioned inside the other petals in the bud), and the remaining petals overlap each other in ascending imbricate aestivation (Judd et al., 2018).

These three subfamilies were traditionally regarded as natural groups, and their recognition was fixed in classical monographs on legumes (Polhill & Raven, 1981; Polhill, 1994; Lewis et al., 2005). Moreover, in some systems (for example, Hutchinson, 1964; Cronquist, 1981), these three groups were treated at the rank of separate families — Papilionaceae, Mimosaceae, and Caesalpiniaceae, respectively (Judd et al., 2018; LPWG, 2017).

2.4. Modern Phylogeny: Paraphyly of Caesalpinioideae and Nesting of Mimosoideae

However, beginning in the 1990s, molecular phylogenetic studies (analysis of sequences of rbcL, matK, trnL, and other plastid and nuclear markers) unambiguously showed that the traditional division into three subfamilies does not reflect the real phylogeny of the family (LPWG, 2017; Judd et al., 2018; Doyle et al., 1997; Bruneau et al., 2008; LPWG, 2013a).

The key conclusions of these studies can be formulated as follows:

1. Caesalpinioideae in the traditional sense is a paraphyletic group. This means that the last common ancestor of all caesalpinioids gave rise not only to them but also to representatives of the other two subfamilies — Mimosoideae and Faboideae (LPWG, 2017; Judd et al., 2018). In other words, “caesalpinioids” are not a clade but a grade — a set of successively branching lineages that do not form a single monophyletic group.

2. Mimosoideae is a monophyletic group, but it is nested within paraphyletic Caesalpinioideae. This means that the closest relatives of mimosoids are not other mimosoids but certain caesalpinioids (LPWG, 2017; Bruneau et al., 2008; Manzanilla & Bruneau, 2012). Molecular data show that mimosoids originated from ancestors belonging to the so-called MCC clade (Mimosoideae-Caesalpinieae-Cassieae), and their closest relatives are certain genera of caesalpinioids, for example, Dimorphandra, Peltophorum, Caesalpinia, and others (Doyle, 2011, 2012; LPWG, 2017).

3. Faboideae (Papilionoideae) is a monophyletic group, which, however, is also nested within paraphyletic Caesalpinioideae s.l. (LPWG, 2017; Judd et al., 2018). The sister groups of Faboideae are certain caesalpinioids (for example, Dialium and related genera), not mimosoids.

4. Basal lineages of the family. Phylogenetic analyses show that the first to branch from the common legume stem are several small clades traditionally assigned to Caesalpinioideae: Cercis + Bauhinia (clade Cercideae), Detarieae (including Hymenaea, Brownea, Amherstia, Tamarindus, and others), Duparquetia (monotypic genus), and Dialioideae (Dialium, Apuleia, Zenia, and others) (LPWG, 2017; Bruneau et al., 2008). It is these groups, together with Faboideae and redefined Caesalpinioideae (including mimosoids), that constitute the six subfamilies of the new classification.

Thus, the phylogenetic structure of the family Fabaceae can be schematically represented as follows (LPWG, 2017; Judd et al., 2018):

Fabaceae:

• Cercidoideae (Cercis, Bauhinia, and relatives)
• Detarioideae (Hymenaea, Brownea, Amherstia, Tamarindus, etc.)
• Duparquetioideae (Duparquetia orchidacea)
• Dialioideae (Dialium, Apuleia, Zenia, etc.)
• Clade uniting: Caesalpinioideae (in the new sense, including Mimosoideae) and Faboideae (Papilionoideae).

This scheme reflects the successive branching of basal clades and the existence of a large clade uniting redefined Caesalpinioideae (with mimosoids) and Faboideae.

2.5. New LPWG (2017) Classification: Six Subfamilies

In 2017, the Legume Phylogeny Working Group (LPWG) published a new classification of the family Leguminosae, based on the most complete phylogenetic analysis to date, including sequences of the matK gene for 3842 samples representing 3696 species and 698 of 765 genera of the family (LPWG, 2017). This classification recognizes six subfamilies, each of which is monophyletic and well supported by both molecular and morphological data (LPWG, 2017; Judd et al., 2018).

Let us list these six subfamilies in order of their divergence from the common stem (LPWG, 2017):

2.6. Key Morphological Characters for Identification of Subfamilies

For practical identification of subfamilies, the following key can be used (LPWG, 2017; Judd et al., 2018):

1. Leaves bipinnate; seeds usually with an open or closed pleurogram on both sides — Caesalpinioideae (in the new sense, including the mimosoid clade).

1. Leaves never bipinnate; seeds without a pleurogram — 2.

2. Leaves unifoliolate, bilobed or entire, or compound and bifoliolate; seed hilum rounded or semilunar — 3.

2. Leaves various; if simple or bifoliolate, then seed hilum not semilunar and rarely rounded — 4.

3. Extrafloral nectaries and other glandular structures (if present) on the lower surface or margin of leaflets; stipules usually intrapetiolar (free or fused), rarely lateral — Detarioideae.

3. Extrafloral nectaries absent or present on the petiole or rachis; stipules lateral and free or absent — Cercidoideae.

4. Inflorescences strongly branched, thyrsoid, or racemes with two-ranked arrangement of flowers; leaves usually odd-pinnate with alternate leaflets; extrafloral nectaries on petiole or rachis absent — Dialioideae.

4. Inflorescences usually racemes with spiral arrangement of flowers, often gathered in branched panicles or condensed into spikes or clusters; leaves usually paripinnate with opposite leaflets, rarely bifoliolate or with alternate leaflets; extrafloral nectaries (if present) on petiole or rachis between pairs of leaflets — Caesalpinioideae (including the mimosoid clade).

5. Flowers usually papilionaceous and zygomorphic, rarely radially symmetrical; median (adaxial) petal outermost, enveloping the other petals in the bud, or petals absent; sepals fused, at least at the base, into a tube or completely enclosing the bud; seeds with a complex hilar valve, pleurogram absent; embryo usually curved — Faboideae (Papilionoideae).

5. Flowers not papilionaceous (if rarely appearing papilionaceous, then median petal innermost), either zygomorphic or radially symmetrical, median (adaxial) petal innermost, or petals valvate (in the mimosoid clade of Caesalpinioideae); sepals free or fused; seeds without a complex hilar valve, with or without a pleurogram; embryo usually straight — Caesalpinioideae (in the broad sense).

This key reflects the main morphological differences between the six subfamilies and can be used to identify genera and species of legumes in the field.

2.7. Evolutionary and Phylogenetic Aspects

The new LPWG (2017) classification reflects not only modern phylogenetic views but also evolutionary trends in the family. Several key points should be noted:

1. Antiquity of the family. Legumes are an ancient group whose fossil remains are known from the Early Cretaceous (about 135 million years ago), and possible origin in the Jurassic (more than 140 million years ago) (Judd et al., 2018; LPWG, 2017). Diversification of the main clades of the family apparently occurred in the Cretaceous and Paleogene (Lavin et al., 2005; LPWG, 2017).

2. Basal lineages. The earliest divergent lineages of the family — Cercidoideae, Detarioideae, Duparquetioideae, and Dialioideae — retained a number of plesiomorphic characters, such as absence of root nodules, often non-papilionaceous flowers, and woody fruits (LPWG, 2017; Bruneau et al., 2008). These groups have predominantly tropical and subtropical distribution.

3. Large clade Caesalpinioideae + Faboideae. The youngest and species-richest clades — redefined Caesalpinioideae (including mimosoids) and Faboideae — demonstrate significant morphological and ecological diversity and include most economically important genera (LPWG, 2017; Judd et al., 2018).

4. Evolution of symbiosis with rhizobia. The ability to form root nodules with nitrogen-fixing bacteria apparently arose several times in legume evolution or was inherited from a common ancestor with subsequent losses in some lineages (Doyle, 2011, 2012; LPWG, 2017). Basal subfamilies (Cercidoideae, Detarioideae, Duparquetioideae, Dialioideae) do not form nodules, whereas Caesalpinioideae (including mimosoids) and Faboideae include both nodulating and non-nodulating species (LPWG, 2017; Sprent, 2007; Lambers & Oliveira, 2019).

5. Morphological evolution of the flower. It was traditionally thought that the papilionaceous flower of Faboideae was the most specialized flower type in the family, and the actinomorphic flowers of Mimosoideae were the most primitive. However, phylogenetic data show that the actinomorphic flowers of mimosoids are derived from zygomorphic ancestors, not the reverse (LPWG, 2017; Judd et al., 2018). This is an example of homoplasy — parallel or convergent origin of similar characters in different lineages.

6. Paraphyly of Caesalpinioideae s.l. and the need for a new classification. It was precisely the paraphyletic nature of traditional Caesalpinioideae and the nesting of Mimosoideae and Faboideae within this grade that served as the main reason for developing the new LPWG (2017) classification. The new system recognizes only monophyletic groups, which corresponds to the principles of phylogenetic systematics (Judd et al., 2018).

2.8. Significance of the New Classification for the Agrosphere

The new LPWG (2017) classification has important practical significance for agronomy, breeding, and plant protection:

1. Accurate identification. Understanding phylogenetic relationships allows more accurate identification of legume genera and species, which is critically important for plant quarantine, seed production, and introduction.

2. Breeding and genetic resources. Knowledge of phylogeny helps identify the closest wild relatives of cultivated species, which can serve as donors of genes for resistance to diseases, pests, and abiotic stresses (Prohens & Nuez, 2008; LPWG, 2017).

3. Symbiotic nitrogen fixation. Understanding the evolution of symbiosis with rhizobia allows targeted selection of effective bacterial strains for seed inoculation and development of strategies for using legumes in crop rotations (Marschner, 2012; Lambers & Oliveira, 2019).

4. Feed production. The new classification helps systematize forage legumes and evaluate their nutritive value and agronomic properties (Connor et al., 2011).

5. Weed plants. Many legumes are weeds (for example, some species of Vicia, Lathyrus, Mimosa). Accurate identification and understanding of their phylogenetic relationships are necessary for developing effective control measures (LPWG, 2017).

3.1. Food Crops of the Old World

3.2. Crops of American Origin

3.3. Crops of East Asian Origin

3.4. Forage Grasses and Pasture Legumes

3.5. Oil Crops

3.6. Other Important Genera

3.7. Summary Table of the Most Important Legume Genera

4.1. General Characteristics of Legume–Rhizobia Symbiosis

Symbiosis is the “joint life” of two or more organisms, often including specialized structures. In a broad sense, symbiotic associations include parasitic and commensal, as well as mutually beneficial partnerships (Lambers & Oliveira, 2019). In this chapter we use the term “symbiosis” in a narrow sense — to denote mutually beneficial associations between plants and microorganisms.

Legumes (Fabaceae) are one of the few groups of higher plants capable of entering into symbiotic relationships with nitrogen-fixing bacteria known as rhizobia (Lambers & Oliveira, 2019; Marschner, 2012). These bacteria are capable of reducing atmospheric molecular nitrogen (N₂) to ammonia (NH₃) using the enzyme nitrogenase. The host plant provides the bacteria with an energy substrate (photosynthates) and a protective environment (nodules), and in return receives nitrogen in available form (Marschner, 2012; Schopfer & Brennicke, 2016).

The ability to form nodules with rhizobia is not universal for all legumes. According to modern estimates, only about 70% of Fabaceae species are capable of forming nodules (Sprent, 2007; LPWG, 2017). This ability is distributed unevenly: it is practically absent in the basal subfamilies (Cercidoideae, Detarioideae, Duparquetioideae, Dialioideae) and is widely represented in Caesalpinioideae (especially in the mimosoid clade) and Faboideae (LPWG, 2017; Sprent, 2007; Lambers & Oliveira, 2019).

4.2. Rhizobia: Taxonomic Diversity and Classification

Rhizobia are a collective group of nitrogen-fixing bacteria capable of forming nodules on the roots of leguminous plants. Initially, all of them were assigned to the genus Rhizobium (Schopfer & Brennicke, 2016), but modern taxonomy based on molecular genetic data (analysis of 16S rRNA sequences and other genes) has shown that rhizobia are a polyphyletic group including representatives of several genera from the classes Alphaproteobacteria and Betaproteobacteria (Marschner, 2012; Lambers & Oliveira, 2019).

4.3. Specificity of Symbiosis: Not All Legumes Form Nodules with Any Rhizobia

Symbiosis between legumes and rhizobia is characterized by high specificity: each rhizobial strain is capable of forming effective nodules only with a certain range of host plants (Marschner, 2012; Lambers & Oliveira, 2019). This specificity is determined by a complex “molecular dialogue” between partners, including exchange of chemical signals (Schopfer & Brennicke, 2016; Lambers & Oliveira, 2019).

4.4. Actinorhizal Symbiosis

Besides rhizobial symbiosis, some non-legume plants form nodules with actinomycetes of the genus *Frankia (Marschner, 2012; Lambers & Oliveira, 2019). This type of symbiosis is called actinorhizal*. It is widespread among about 200 species of woody plants from eight families, predominantly in temperate and subtropical regions (Marschner, 2012; Rubatzky & Yamaguchi, 1997).

The most important genera of actinorhizal plants (Marschner, 2012; Rubatzky & Yamaguchi, 1997):

• Alnus (alder) — Betulaceae;
• Casuarina (casuarina) — Casuarinaceae;
• Hippophae (sea buckthorn) — Elaeagnaceae;
• Elaeagnus (oleaster) — Elaeagnaceae;
• Myrica (bayberry) — Myricaceae;
• Ceanothus — Rhamnaceae;
• Purshia — Rosaceae;
• Rubus — Rosaceae;
• Discaria — Rhamnaceae.

Actinorhizal plants play an important ecological role in forest and shrub ecosystems, especially on nitrogen-poor soils. For example, alder (Alnus spp.) is capable of fixing from 15 to 300 kg N/ha per year, enriching the soil with nitrogen and improving its fertility (Marschner, 2012).

4.5. Evolution of Symbiosis with Nitrogen-Fixing Bacteria

The evolution of symbiosis between plants and nitrogen-fixing bacteria is one of the key problems of modern evolutionary biology. The ability to form nodules arose within the clade Fabids and apparently has a single evolutionary origin with subsequent multiple losses (Soltis et al., 1995; Doyle, 2011, 2012; LPWG, 2017).

4.6. Practical Significance of Symbiotic Nitrogen Fixation

Symbiotic nitrogen fixation is of enormous practical importance for sustainable agriculture. It allows:

1. Reducing dependence on nitrogen fertilizers: legume crops are able to satisfy their nitrogen needs through symbiosis, which reduces the cost of mineral fertilizers and reduces environmental pollution (Connor et al., 2011; Marschner, 2012).

2. Enriching the soil with nitrogen: after harvesting legumes, a significant part of the fixed nitrogen remains in the soil in the composition of root residues and crop residues, enriching it with nitrogen for subsequent crops (Connor et al., 2011; Marschner, 2012).

3. Using legumes as green manure: green manure is an important practice of organic farming that allows enriching the soil with organic matter and nitrogen without applying mineral fertilizers (Connor et al., 2011).

4. Including legumes in crop rotations: scientifically based crop rotations with legumes increase the yield of subsequent crops by 30–35% and more (Connor et al., 2011; Khan et al., 2019).

4.7. Relationship Between Taxonomic Affinity and Nitrogen-Fixation Ability

The ability to form nodules and fix nitrogen correlates with the taxonomic position of legumes (LPWG, 2017; Sprent, 2007; Doyle, 2011):

• Basal subfamilies (Cercidoideae, Detarioideae, Duparquetioideae, Dialioideae) — do not form nodules (LPWG, 2017).
• Caesalpinioideae (in the new sense, including the mimosoid clade) — varies: some genera form nodules (especially in the mimosoid clade), others do not (LPWG, 2017; Sprent, 2007).
• Faboideae — most genera form nodules, although there are exceptions (for example, some species of Lupinus, Astragalus may not form nodules under certain conditions) (LPWG, 2017; Sprent, 2007).

This correlation reflects the evolutionary history of the family: the ability for symbiosis with rhizobia apparently arose in the common ancestor of Caesalpinioideae + Faboideae but was lost in some lineages (Doyle, 2011, 2012; LPWG, 2017).

5.1. Concept of Gene Pools (GP1–GP3)

For effective use of genetic resources in breeding, the concept of gene pools, proposed by Harlan and de Wet (1971) and developed in works on plant genetic resources, is applied (Prohens & Nuez, 2008; Rubatzky & Yamaguchi, 1997). According to this concept, the genetic resources of a species are divided into three main pools:

• Primary gene pool (GP1, primary gene pool) — includes cultivated varieties and wild forms of the same species that easily cross with cultivated plants, produce fertile offspring, and do not require special methods for gene transfer. Genes from GP1 are easily introgressed into cultivated varieties by traditional breeding methods (Prohens & Nuez, 2008).

• Secondary gene pool (GP2, secondary gene pool) — includes closely related species, crossing with which is possible but associated with certain difficulties: partial sterility of hybrids, need for embryo culture, meiotic disturbances. Gene transfer from GP2 requires special methods (Prohens & Nuez, 2008; Rubatzky & Yamaguchi, 1997).

• Tertiary gene pool (GP3, tertiary gene pool) — includes more distant species, crossing with which is possible only using special methods (embryo culture, somatic hybridization, genetic transformation). Hybrids are often sterile or nonviable (Prohens & Nuez, 2008).

This classification allows breeders to assess how easily useful genes can be transferred from a wild relative into a cultivated variety.

5.2. Soybean: Glycine soja — Wild Ancestor

Systematic position: Glycine max (L.) Merr. — cultivated soybean — belongs to the subgenus Soja of the genus Glycine Willd. (subfamily Faboideae, tribe Phaseoleae, subtribe Glycininae) (Rubatzky & Yamaguchi, 1997; Prohens & Nuez, 2008). The wild ancestor of soybean — Glycine soja Siebold & Zucc. — is an annual growing in East Asia (China, Korea, Japan, Russia — Far East) (Rubatzky & Yamaguchi, 1997).

Gene pools of soybean:

• GP1: G. max (cultivated soybean) and G. soja (wild soybean) — cross freely, produce fertile offspring (Prohens & Nuez, 2008; Rubatzky & Yamaguchi, 1997).
• GP2: species of the subgenus Glycine (for example, G. canescens, G. tomentella) — crossing possible but with difficulties (Prohens & Nuez, 2008).
• GP3: more distant species of the genus Glycine — crossing requires special methods (Prohens & Nuez, 2008).

Significance of G. soja for breeding:

Glycine soja possesses a number of valuable traits lost during domestication (Prohens & Nuez, 2008; Rubatzky & Yamaguchi, 1997):

• Disease resistance: G. soja shows resistance to soybean cyst nematode (Heterodera glycines), downy mildew (Peronospora manshurica), brown spot (Septoria glycines), soybean mosaic virus (SMV), and other pathogens (Prohens & Nuez, 2008).
• Pest resistance: G. soja is resistant to soybean pod borer (Leguminivora glycinivorella), spider mite (Tetranychus urticae), and other pests (Prohens & Nuez, 2008).
• Resistance to abiotic stresses: G. soja is more resistant to drought, salinity, and low temperatures than cultivated soybean (Prohens & Nuez, 2008; Pessarakli, 2020).
• Seed quality: G. soja has higher protein content (up to 50%) and a more favorable amino acid composition than many cultivated varieties (Prohens & Nuez, 2008).

Soybean breeding programs actively use G. soja for introgression of genes for resistance to nematodes, diseases, and abiotic stresses (Prohens & Nuez, 2008; Rubatzky & Yamaguchi, 1997). For example, genes for resistance to soybean cyst nematode (SCN) were transferred from G. soja into cultivated varieties and are widely used in breeding (Prohens & Nuez, 2008).

5.3. Bean: Wild Species of Phaseolus

Systematic position: The genus Phaseolus L. (subfamily Faboideae, tribe Phaseoleae) includes about 50–60 species distributed in the Neotropics (Prohens & Nuez, 2008; Rubatzky & Yamaguchi, 1997). Cultivated species: P. vulgaris, P. lunatus, P. coccineus, P. acutifolius, P. polyanthus (Prohens & Nuez, 2008).

Gene pools of bean:

• GP1: P. vulgaris (cultivated bean) and its wild forms P. vulgaris var. aborigineus — cross freely (Prohens & Nuez, 2008; Gepts, 1998).
• GP2: P. coccineus, P. costaricensis, P. polyanthus — crossing possible, but hybrids partially sterile (Prohens & Nuez, 2008; Singh, 2001).
• GP3: P. acutifolius (tepary bean), P. parvifolius — crossing requires embryo culture (Prohens & Nuez, 2008; Singh, 2001).

Significance of wild Phaseolus species for breeding:

Wild Phaseolus species possess valuable traits actively used in breeding (Prohens & Nuez, 2008; Singh, 2001):

• P. vulgaris var. aborigineus (wild bean): resistance to anthracnose (Colletotrichum lindemuthianum), common bacterial blight (Xanthomonas axonopodis pv. phaseoli), fusarium wilt (Fusarium oxysporum f. sp. phaseoli), bean common mosaic virus (BCMV) (Prohens & Nuez, 2008; Pessarakli, 2020).

• P. acutifolius (tepary bean): unique resistance to drought and high temperatures, resistance to common bacterial blight, bean golden mosaic virus (BGMV), fusarium wilt (Prohens & Nuez, 2008; Rubatzky & Yamaguchi, 1997). Genes for resistance to bacterial blight from P. acutifolius have been successfully transferred into P. vulgaris (Singh, 2001).

• P. coccineus (scarlet runner bean): resistance to anthracnose, fusarium wilt, common mosaic virus, and also to cold (Prohens & Nuez, 2008).

• P. lunatus (lima bean): resistance to drought, high temperatures, bacterial and fungal diseases (Prohens & Nuez, 2008).

Bean breeding programs actively use wild species for introgression of genes for resistance to diseases, pests, and abiotic stresses (Prohens & Nuez, 2008; Singh, 2001; Pessarakli, 2020). For example, genes for resistance to anthracnose (Co-1 – Co-10) were transferred from wild forms of P. vulgaris and P. coccineus (Prohens & Nuez, 2008; Pessarakli, 2020).

5.4. Pea: Pisum sativum subsp. elatius

Systematic position: Pisum sativum L. (subfamily Faboideae, tribe Fabeae) — the only cultivated species of the genus Pisum L. (Rubatzky & Yamaguchi, 1997; Prohens & Nuez, 2008). Wild forms of pea belong to the subspecies P. sativum subsp. elatius (Bieb.) Asch. & Graebn., P. sativum subsp. syriacum (Boiss. & Noë) Berger, P. sativum subsp. asiaticum Govorov (Prohens & Nuez, 2008).

Gene pools of pea:

• GP1: P. sativum subsp. sativum (cultivated pea) and P. sativum subsp. elatius, P. sativum subsp. syriacum — cross freely, produce fertile offspring (Prohens & Nuez, 2008).
• GP2: P. fulvum Sibth. & Sm. — crossing possible but with difficulties (Prohens & Nuez, 2008).
• GP3: other species of the genus Pisum — crossing requires special methods (Prohens & Nuez, 2008).

Significance of P. sativum subsp. elatius for breeding:

Wild pea P. sativum subsp. elatius possesses valuable traits (Prohens & Nuez, 2008; Pessarakli, 2020):

• Disease resistance: resistance to downy mildew (Peronospora pisi), fusarium wilt (Fusarium oxysporum f. sp. pisi), ascochyta blight (Ascochyta pisi, A. pinodes), rust (Uromyces pisi), bacterial blight (Pseudomonas syringae pv. pisi) (Prohens & Nuez, 2008; Pessarakli, 2020).
• Pest resistance: resistance to pea aphid (Acyrthosiphon pisum), pea weevil (Bruchus pisorum), pea moth (Cydia nigricana) (Prohens & Nuez, 2008).
• Resistance to abiotic stresses: resistance to drought, high temperatures, salinity (Prohens & Nuez, 2008; Pessarakli, 2020).

Genes for resistance to fusarium wilt (Fw, Fwf), downy mildew (er1, er2, Er3), ascochyta blight (Rap2, Rmp1–Rmp4) have been identified in wild pea forms and are actively used in breeding (Prohens & Nuez, 2008; Pessarakli, 2020).

5.5. Chickpea: Cicer reticulatum

Systematic position: Cicer arietinum L. (subfamily Faboideae, tribe Cicereae) — the only cultivated species of the genus Cicer L. (Rubatzky & Yamaguchi, 1997; Prohens & Nuez, 2008). The wild ancestor of chickpea — Cicer reticulatum Ladizinsky — is an annual growing in southeastern Turkey (Prohens & Nuez, 2008).

Gene pools of chickpea:

• GP1: C. arietinum (cultivated chickpea) and C. reticulatum (wild chickpea) — cross freely, produce fertile offspring (Prohens & Nuez, 2008).
• GP2: C. echinospermum P.H. Davis — crossing possible but with difficulties (Prohens & Nuez, 2008).
• GP3: other species of the genus Cicer (about 40 species) — crossing requires special methods (Prohens & Nuez, 2008).

Significance of C. reticulatum for breeding:

Cicer reticulatum possesses valuable traits (Prohens & Nuez, 2008; Pessarakli, 2020):

• Disease resistance: resistance to ascochyta blight (Ascochyta rabiei), fusarium wilt (Fusarium oxysporum f. sp. ciceris), root rots (Rhizoctonia solani, Pythium spp.), botrytis (Botrytis cinerea) (Prohens & Nuez, 2008; Pessarakli, 2020).
• Pest resistance: resistance to cotton bollworm (Helicoverpa armigera), chickpea leaf miner (Liriomyza cicerina), chickpea bruchid (Callosobruchus chinensis) (Prohens & Nuez, 2008).
• Resistance to abiotic stresses: resistance to drought, high temperatures, salinity (Prohens & Nuez, 2008; Pessarakli, 2020).

Genes for resistance to ascochyta blight, fusarium wilt, and other diseases have been identified in C. reticulatum and are actively used in chickpea breeding (Prohens & Nuez, 2008; Pessarakli, 2020).

5.6. Alfalfa: Medicago sativa Complex

Systematic position: Medicago sativa L. (subfamily Faboideae, tribe Trifolieae) — a perennial forage crop including several subspecies: M. sativa subsp. sativa (alfalfa), M. sativa subsp. falcata (sickle alfalfa), M. sativa subsp. glomerata (clustered alfalfa), M. sativa subsp. varia (variable alfalfa) (Rubatzky & Yamaguchi, 1997; Prohens & Nuez, 2008).

Gene pools of alfalfa:

• GP1: M. sativa subsp. sativa, M. sativa subsp. falcata, M. sativa subsp. glomerata, M. sativa subsp. varia — cross freely, produce fertile offspring (Prohens & Nuez, 2008).
• GP2: M. coerulea Less. ex Ledeb., M. glutinosa M.Bieb., M. prostrata Jacq. — crossing possible but with difficulties (Prohens & Nuez, 2008).
• GP3: other species of the genus Medicago (about 85 species) — crossing requires special methods (Prohens & Nuez, 2008).

Significance of wild Medicago species for breeding:

Wild Medicago species possess valuable traits (Prohens & Nuez, 2008; Pessarakli, 2020):

• Disease resistance: resistance to fusarium wilt (Fusarium oxysporum f. sp. medicaginis), verticillium wilt (Verticillium albo-atrum), root rots (Phytophthora megasperma, Pythium spp.), anthracnose (Colletotrichum trifolii), common leaf spot (Pseudopeziza medicaginis) (Prohens & Nuez, 2008; Pessarakli, 2020).
• Pest resistance: resistance to alfalfa weevil (Hypera postica), pea aphid (Acyrthosiphon pisum), lygus bug (Lygus spp.), nematodes (Meloidogyne spp., Pratylenchus spp.) (Prohens & Nuez, 2008).
• Resistance to abiotic stresses: resistance to drought, salinity, low temperatures, soil acidity (Prohens & Nuez, 2008; Pessarakli, 2020).

Genes for resistance to fusarium wilt, verticillium wilt, anthracnose, and nematodes have been identified in wild Medicago species and are actively used in alfalfa breeding (Prohens & Nuez, 2008; Pessarakli, 2020).

5.7. Gene Pools GP1–GP3 and Their Use in Breeding

The concept of gene pools (GP1–GP3) is of important practical significance for legume breeding (Prohens & Nuez, 2008; Rubatzky & Yamaguchi, 1997):

GP1 — the most accessible pool for breeding. Genes from GP1 can be transferred by traditional breeding methods (hybridization, selection). Examples: use of wild soybean G. soja for introgression of nematode resistance genes into cultivated soybean; use of wild forms of P. vulgaris for introgression of anthracnose resistance genes (Prohens & Nuez, 2008; Singh, 2001).

GP2 — requires special methods to overcome crossing barriers: embryo culture, ovary culture, use of bridge crosses. Examples: use of P. coccineus for transfer of cold resistance genes into P. vulgaris; use of C. echinospermum for transfer of ascochyta resistance genes into chickpea (Prohens & Nuez, 2008).

GP3 — the most difficult pool for breeding. Requires genetic transformation, somatic hybridization, or embryo culture. Examples: use of P. acutifolius for transfer of bacterial blight resistance genes into P. vulgaris (Singh, 2001); use of distant Medicago species for transfer of drought resistance genes (Prohens & Nuez, 2008).

5.8. Strategies for Using Wild Relatives in Breeding

Modern strategies for using wild relatives in legume breeding include (Prohens & Nuez, 2008; Pessarakli, 2020):

1. Introgression of resistance genes: transfer of genes for resistance to diseases, pests, and abiotic stresses from wild species into cultivated varieties by hybridization, backcrossing, and selection.

2. Gene pyramiding: combining in one genotype several resistance genes to different pathogen races to create durable resistance.

3. Creation of synthetic varieties: use of wild species to create synthetic populations with a broad genetic base.

4. Marker-assisted selection (MAS): use of molecular markers linked to resistance genes to accelerate the breeding process and increase its efficiency (Pessarakli, 2020; Hollingsworth et al., 1999).

5. Genomic selection: use of whole-genome data to predict the breeding value of genotypes and accelerate the breeding process (Pessarakli, 2020).

6. Genetic transformation: direct transfer of resistance genes from wild species into cultivated varieties by genetic engineering (Prohens & Nuez, 2008).

5.9. Problems and Limitations of Using Wild Relatives

The use of wild relatives in breeding is associated with a number of problems and limitations (Prohens & Nuez, 2008; Pessarakli, 2020):

1. Crossing barriers: difficulties in hybridization between cultivated and wild species, partial or complete sterility of hybrids.

2. Linkage drag: resistance genes may be linked to undesirable traits (small seeds, pod shattering, low yield), requiring lengthy backcrosses to eliminate them.

3. Genetic variability of pathogens: high variability of pathogens can overcome resistance transferred from wild species.

4. Energy costs: resistance may be associated with energy costs that reduce yield in the absence of the pathogen.

5. Limited genetic resources: many wild relatives are endangered due to habitat destruction, requiring their conservation ex situ and in situ.

6.1. Identification of species and varieties

Accurate identification of legume species and varieties is of fundamental importance for seed production, plant quarantine, breeding, product quality assessment, and scientific research (Sharma, 2009; Judd et al., 2018). Errors in identification can lead to serious economic losses, the spread of diseases and pests, and a decrease in yield and product quality.

6.2. Quarantine objects among legumes

Plant quarantine is a system of measures aimed at preventing the introduction and spread of dangerous pests, diseases, and weeds (Pessarakli, 2020). Legumes, as important agricultural crops, are subject to quarantine supervision. Many pathogens and pests of legumes are included in national and international quarantine lists (Pessarakli, 2020; Prohens & Nuez, 2008).

6.3. Breeding for resistance to diseases and pests

Breeding for resistance to diseases and pests is one of the priority areas in breeding legume crops (Pessarakli, 2020; Prohens & Nuez, 2008). Resistant varieties make it possible to reduce yield losses, decrease the use of pesticides, lower costs, and reduce the negative impact on the environment.

6.4. Assessment of forage and food qualities

Systematics and taxonomy play an important role in assessing the forage and food qualities of legumes, since different species and varieties differ substantially in chemical composition, nutritional value, and the presence of antinutritional factors (Rubatzky & Yamaguchi, 1997; Connor et al., 2011).

6.5. Weedy legumes and their control

Many legume species are dangerous weeds clogging crops of agricultural plants, including legumes themselves (Pessarakli, 2020; Rubatzky & Yamaguchi, 1997). Weedy legumes reduce yield, complicate harvesting, worsen product quality, and can be toxic to animals and humans.

7.1. Fabaceae — a unique family combining enormous diversity and a key role in sustainable agriculture

Over seven lectures, we have examined one of the most amazing and significant families of flowering plants — Fabaceae, or Leguminosae. This family, numbering about 770 genera and more than 19,500 species, ranks third among all flowering plant families in number of species, yielding only to Asteraceae and Orchidaceae (LPWG, 2017; Judd et al., 2018). Legumes are distributed cosmopolitically — from Arctic tundras to tropical rain forests, from deserts to wetlands — and are represented by all life forms: from large tropical emergent trees to herbaceous annuals of temperate latitudes, from lianas to succulents (Schrire et al., 2005a, b; LPWG, 2017).

This diversity reflects the broad ecological plasticity of the family and its ability to adapt to the most varied environmental conditions. Legumes dominate in dry tropical forests and savannas, play a key role in Mediterranean, desert, and temperate communities, and reach high latitudes and altitudes (LPWG, 2017). They are among the most important ecological components of virtually all terrestrial ecosystems.

The economic importance of legumes is difficult to overestimate. In economic significance, the family is second only to Poaceae (grasses) (LPWG, 2017). Legumes provide humanity with:

• Food protein — grain legumes (pea, common bean, soybean, chickpea, lentil, peanut) contain 20–50% protein and are the most important source of plant protein (Rubatzky & Yamaguchi, 1997; Prohens & Nuez, 2008);
• Vegetable oil — soybean and peanut are the most important oilseed crops in the world (Rubatzky & Yamaguchi, 1997);
• Animal feed — alfalfa, clover, sainfoin, and vetch are the basis of forage production in temperate latitudes (Connor et al., 2011);
• Industrial raw materials — wood, tannins, gums, dyes, medicines, essential oils (LPWG, 2017);
• Ornamental plants — robinia, wisteria, lupine, delonix, bauhinia (LPWG, 2017).

However, the main unique feature of legumes is their ability for symbiotic nitrogen fixation — the process by which atmospheric molecular nitrogen is converted into forms available to plants with the help of rhizobia bacteria living in nodules on the roots (Marschner, 2012; Lambers & Oliveira, 2019). This ability makes legumes indispensable components of sustainable agroecosystems, since they not only satisfy their own nitrogen needs but also enrich the soil with nitrogen available to subsequent crops (Connor et al., 2011; Marschner, 2012).

On a global scale, biological nitrogen fixation provides about 60% of all nitrogen entering terrestrial ecosystems, with symbiotic nitrogen fixation by legumes accounting for about 50% of this amount — approximately 40–70 million tons of nitrogen per year (Herridge et al., 2008; Marschner, 2012). For comparison: industrial production of nitrogen fertilizers provides about 100 million tons of nitrogen per year (Connor et al., 2011). Thus, symbiotic nitrogen fixation by legumes is a renewable nitrogen resource that can reduce agriculture's dependence on fossil fuels and decrease the negative impact on the environment.

7.2. Understanding phylogeny and symbiotic relationships is necessary for breeding and agricultural technologies

Modern legume systematics has undergone revolutionary changes over the past two decades. The traditional division of the family into three subfamilies — Faboideae (Papilionoideae), Mimosoideae, and Caesalpinioideae — turned out to be untenable from the standpoint of phylogeny: molecular phylogenetic studies have unequivocally shown that Caesalpinioideae in the traditional sense are paraphyletic, and Mimosoideae are nested within them (LPWG, 2017; Judd et al., 2018; Doyle et al., 1997; Bruneau et al., 2008).

The new classification of LPWG (2017), based on the most complete phylogenetic analysis, recognizes six monophyletic subfamilies:

1. Cercidoideae — 12 genera, about 335 species;

2. Detarioideae — 84 genera, about 760 species;

3. Duparquetioideae — 1 genus, 1 species;

4. Dialioideae — 17 genera, about 85 species;

5. Caesalpinioideae (in the new sense, including the mimosoid clade) — 148 genera, about 4400 species;

6. Faboideae (Papilionoideae) — 503 genera, about 14,000 species.

This classification reflects not only modern phylogenetic concepts but also evolutionary trends in the family. The basal subfamilies (Cercidoideae, Detarioideae, Duparquetioideae, Dialioideae) do not form root nodules and have retained a number of plesiomorphic characters; the youngest and most species-rich clades — the redefined Caesalpinioideae (including the mimosoid clade) and Faboideae — demonstrate significant morphological and ecological diversity and include most economically important genera (LPWG, 2017; Judd et al., 2018).

Understanding legume phylogeny is of the utmost practical importance for breeding and agricultural technologies:

• Accurate identification. Understanding phylogenetic relationships allows more accurate identification of legume genera and species, which is critically important for plant quarantine, seed production, and introduction (Pessarakli, 2020; Sharma, 2009).

• Breeding and genetic resources. Knowledge of phylogeny helps identify the closest wild relatives of cultivated species, which can serve as donors of genes for resistance to diseases, pests, and abiotic stresses (Prohens & Nuez, 2008; LPWG, 2017).

• Symbiotic nitrogen fixation. Understanding the evolution of symbiosis with rhizobia makes it possible to purposefully select effective bacterial strains for seed inoculation and to develop strategies for using legumes in crop rotations (Marschner, 2012; Lambers & Oliveira, 2019).

• Forage production. The new classification helps systematize forage legumes and assess their nutritional value and agronomic properties (Connor et al., 2011).

• Weedy plants. Many legumes are weeds (for example, some species of Vicia, Lathyrus, Mimosa). Accurate identification and understanding of their phylogenetic relationships are necessary for developing effective control measures (Pessarakli, 2020; LPWG, 2017).

The symbiosis of legumes with rhizobia is a unique ability that determines their role in the nitrogen cycle and sustainable agriculture. Rhizobia are a polyphyletic group of nitrogen-fixing bacteria including representatives of Alphaproteobacteria (Rhizobium, Bradyrhizobium, Sinorhizobium, Mesorhizobium, etc.) and Betaproteobacteria (Burkholderia, Cupriavidus) (Marschner, 2012; Lambers & Oliveira, 2019). The specificity of the symbiosis is determined by a complex molecular dialogue between the partners, including the exchange of flavonoids and Nod factors (Schopfer & Brennicke, 2016; Lambers & Oliveira, 2019).

In the evolution of symbiosis, the predisposition to form nodules arose once within Fabids and has a common origin with arbuscular mycorrhizal symbiosis (Soltis et al., 1995; Doyle, 2011, 2012). Multiple losses of the ability for symbiosis occurred in different legume lineages, especially in the basal subfamilies (Doyle, 2011, 2012; LPWG, 2017). The practical importance of symbiotic nitrogen fixation is enormous: it makes it possible to reduce dependence on nitrogen fertilizers, enrich the soil with nitrogen, use legumes as green manure, and include them in crop rotations (Connor et al., 2011; Marschner, 2012).

7.3. Wild relatives — a strategic resource for the future

Wild relatives of cultivated legumes represent a strategic resource for the future of breeding, ensuring the resistance and adaptability of cultivated varieties under conditions of a changing climate and increasing pressure from pathogens (Prohens & Nuez, 2008; Pessarakli, 2020).

The concept of gene pools (GP1–GP3) makes it possible to classify genetic resources according to the ease of their use in breeding (Harlan & de Wet, 1971; Prohens & Nuez, 2008):

• GP1 — cultivated varieties and wild forms of the same species, which cross easily with cultivated plants;
• GP2 — closely related species with which crossing is possible but associated with difficulties;
• GP3 — distant species with which crossing requires special methods.

We examined the most important examples of the use of wild relatives in legume breeding:

• Soybean: Glycine soja — the wild ancestor, possessing resistance to nematodes, diseases, and abiotic stresses (Prohens & Nuez, 2008; Rubatzky & Yamaguchi, 1997);
• Common bean: wild species of Phaseolus (P. vulgaris var. aborigineus, P. acutifolius, P. coccineus, P. lunatus) — sources of genes for resistance to anthracnose, bacterial diseases, and drought (Prohens & Nuez, 2008; Singh, 2001);
• Pea: Pisum sativum subsp. elatius — a source of genes for resistance to Fusarium, downy mildew, and Ascochyta blight (Prohens & Nuez, 2008; Pessarakli, 2020);
• Chickpea: Cicer reticulatum — a source of genes for resistance to Ascochyta blight, Fusarium, and drought (Prohens & Nuez, 2008; Pessarakli, 2020);
• Alfalfa: wild species of Medicago — sources of genes for resistance to Fusarium, Verticillium, nematodes, and drought (Prohens & Nuez, 2008; Pessarakli, 2020).

Strategies for using wild relatives include introgression of resistance genes, gene pyramiding, marker-assisted selection (MAS), genomic selection, and genetic transformation (Pessarakli, 2020; Prohens & Nuez, 2008; Hollingsworth et al., 1999). However, the use of wild relatives is associated with a number of problems: crossing barriers, linkage of undesirable traits, variability of pathogens, and limited genetic resources (Prohens & Nuez, 2008; Pessarakli, 2020).

Conservation of legume genetic resources is one of the key tasks of modern agronomy and plant genetics. Genetic banks such as CIAT (Centro Internacional de Agricultura Tropical), ICARDA (International Center for Agricultural Research in the Dry Areas), ICRISAT (International Crops Research Institute for the Semi-Arid Tropics), and others preserve tens of thousands of accessions of cultivated and wild legumes (Rubatzky & Yamaguchi, 1997; Prohens & Nuez, 2008). These collections serve as the basis for breeding new resistant and productive varieties.

7.4. Prospects for further study and use of legumes

Legumes remain one of the most actively studied groups of plants. Modern research is conducted in several key directions:

1. Phylogeny and systematics. Refinement of phylogenetic relationships within the family continues using whole-genome data (phylogenomics), which will make it possible to create a more detailed and stable classification (LPWG, 2017; Judd et al., 2018).

2. Genomics and molecular biology. Sequencing of the genomes of the most important legume crops (soybean, common bean, pea, chickpea, alfalfa) opens new possibilities for identifying genes for economically valuable traits and for marker-assisted selection (Pessarakli, 2020; Hollingsworth et al., 1999).

3. Symbiotic nitrogen fixation. Study of the molecular mechanisms of symbiosis, specificity, and evolution of nodules makes it possible to develop strategies for increasing the efficiency of nitrogen fixation and expanding the range of plants capable of symbiosis (Doyle, 2011, 2012; Lambers & Oliveira, 2019; Van Velzen et al., 2019).

4. Breeding for resistance. Development of new breeding methods (genomic selection, genome editing using CRISPR/Cas9) makes it possible to accelerate the creation of varieties resistant to diseases, pests, and abiotic stresses (Pessarakli, 2020).

5. Sustainable agriculture. Integration of legumes into crop rotations, use of green manure, green fertilization, and biological nitrogen fixation are key elements of sustainable agriculture that reduces dependence on mineral fertilizers and pesticides (Connor et al., 2011).

6. Climate change. Legumes, owing to their ability for nitrogen fixation and broad ecological plasticity, can play an important role in adapting agriculture to climate change (Pessarakli, 2020; Connor et al., 2011).

7. Food security. Legumes are the most important source of plant protein for the population of developing countries. Increasing the yield and resistance of legume crops is a key task for ensuring food security (Rubatzky & Yamaguchi, 1997; Prohens & Nuez, 2008).

7.5. Final provisions of the course

Summarizing the entire course of lectures on legume systematics, the following key provisions can be formulated:

1. Fabaceae is the third largest family of flowering plants, numbering about 770 genera and more than 19,500 species, distributed cosmopolitically and represented by all life forms (LPWG, 2017; Judd et al., 2018).

2. The monophyly of the family is reliably confirmed by molecular and morphological data; its closest relatives are the families Polygalaceae, Surianaceae, and Quillajaceae within the order Fabales (Judd et al., 2018; LPWG, 2017).

3. The new classification of LPWG (2017) recognizes six monophyletic subfamilies: Cercidoideae, Detarioideae, Duparquetioideae, Dialioideae, Caesalpinioideae (including the mimosoid clade), and Faboideae. The traditional division into three subfamilies does not reflect the real phylogeny (LPWG, 2017).

4. Legumes play a key role in human nutrition, animal feeding, and sustainable agriculture owing to their high content of protein and oil and their ability for symbiotic nitrogen fixation (Rubatzky & Yamaguchi, 1997; Connor et al., 2011; Marschner, 2012).

5. Symbiosis with rhizobia is a unique ability of legumes that allows them to fix atmospheric nitrogen and enrich the soil. The specificity of the symbiosis is determined by a molecular dialogue between the partners; the evolution of symbiosis has a single origin within Fabids with multiple losses (Doyle, 2011, 2012; Lambers & Oliveira, 2019).

6. Wild relatives of cultivated legumes are a strategic resource for breeding for resistance to diseases, pests, and abiotic stresses; their conservation and rational use is a key task of modern agronomy (Prohens & Nuez, 2008; Pessarakli, 2020).

7. Practical use of legume systematics includes identification of species and varieties, quarantine control, breeding for resistance, assessment of forage and food qualities, and control of weedy legumes (Pessarakli, 2020; Sharma, 2009; Rubatzky & Yamaguchi, 1997).

8. Modern studies of legumes are conducted using phylogenomics, genomics, molecular biology, and genome editing methods, which opens new prospects for breeding and sustainable agriculture (Pessarakli, 2020; Hollingsworth et al., 1999).

7.6. Concluding remarks

Legumes are an amazing family combining enormous diversity, unique biological features, and a key role in sustainable agriculture. From tropical emergent trees to herbaceous annuals of temperate latitudes, from food crops to forage grasses, from symbiotic nitrogen fixers to ornamental plants, legumes have accompanied humanity throughout its history and will play a most important role in the future.

Understanding the phylogeny, systematics, and symbiotic relationships of legumes is necessary for:

• Breeding new resistant and productive varieties;
• Agricultural technologies based on biological nitrogen fixation and sustainable agriculture;
• Conservation of biodiversity and genetic resources;
• Ensuring food security and sustainable development.

Wild relatives of cultivated legumes are a strategic resource for the future, and their conservation is one of the key tasks of modern science and practice. As E.J.H. Corner (1976) wrote: “We await the treatise that will bring the herbarium to life into a living tree of phylogeny.” Modern legume systematics, armed with molecular methods and a phylogenetic approach, is making this treatise a reality.

Legumes are not just a plant family. They are the basis of sustainable agriculture, a source of food for billions of people, a key element of the nitrogen cycle, and a strategic resource for the future of humanity. Their study and rational use is a task worthy of the attention of the entire scientific community.