The legume family (Fabaceae) is one of the largest families of flowering plants with more than 19,500 species [1
] and an estimated 732–765 genera [3
]. The well-known symbiotic relationship between legumes and root-nodule bacteria (hereafter, rhizobia) supplies biologically fixed nitrogen (BNF) to natural and agroecosystems around the globe [6
]. BNF, which may be considered the most fundamentally important biological process on earth aside from photosynthesis [7
], reduces more than 100 Tg dinitrogen to ammonia each year [8
]. This form of nitrogen (N) is directly useable by legumes, and eventually, through nutrient cycling and consumption, becomes available to other plants and organisms. In fact, the entire nutritional N requirement for humans is obtained directly or indirectly from plants [9
]. For this reason, legumes have long been exploited in agriculture as essential rotational species in cropping systems to improve soil fertility and increase annual cereal yields, and they continue to supply approximately 13% of the annual global agricultural N requirements (30–50 Tg) [10
]. In addition to the direct benefits of BNF, annual grain legumes are second only to cereals (Poaceae) in economic importance as food crops, and perennial herbaceous legumes are some of the most nutritious forages for livestock [1
]. Despite all their benefits, less than 15 species of grain legumes and 50 forage legumes are globally traded and commercially important. This suggests that thousands of species may have been overlooked for their potential utility to humans and unique adaptations to their native environments [7
Domestication and development of new or alternative legume crops could increase crop diversity and reduce human reliance on only a few major food crops, and if done thoughtfully, could improve the resilience and sustainability of food production [13
]. Replacing annual with perennial grain crops has been proposed as a solution to improve food and ecosystem security [14
]. In contrast to annuals, the deep, extensive root systems and longer growing season of perennials allows them to have increased capacity to capture sunlight and sequester carbon, to reduce moisture and nutrient loss through leaching and/or runoff, and to prevent soil erosion [15
]. Therefore, new perennial grain legumes, with novel eco-physiological attributes and nutritional properties (i.e., high oil, high protein, high fiber content) similar to those of their annual counterparts, would be valuable additions to the handful of grain legume crops used in modern, sustainable agriculture.
The benefit of including legumes in cropping systems depends on effective nodulation by rhizobia, total BNF and N use efficiency (NUE) [18
]. Perennials may have distinct advantages over annuals in this capacity. In annual legume systems, the rhizobia symbiosis must be reestablished every growing season; therefore, the symbiosis only exists for a portion of the plant’s lifecycle. As a result, the symbiosis may not wholly supply the annual grain legume’s inorganic N requirement and often does little to improve soil N or nutrient status because nearly all BNF N and plant resources are mobilized and translocated to the seed [19
]. Conversely for perennial grain legumes, the symbiosis exists and functions during the entirety of each growing season. As a result, perennial legumes benefit from the rhizobia-symbiosis for a much greater proportion of their lifespan; and therefore, are expected to have greater annual rates of BNF and to supply a larger fraction of their inorganic N requirements without further depleting soil N levels. Perennial grain legume production is also likely to have a better NUE than using annual legumes grown as cover crops to supply N to cereal grains. Perennial grain legumes retain the natural synchronicity of N supply and demand during grain fill and have small rates of N loss in the cropping system [17
]. In annual cereal grain systems with an annual legume cover crop, the legume may fail to meet the cereal grain’s N requirements because the rhizobia-symbiosis exists for only a fraction of the growing season, because using tillage to terminate the legume cover crop can change the carbon-nitrogen balance, because loss of N from the soil occurs due to its volatility and mobility and because complete synchronicity of the legume N supply and the cereal grain N demand is extremely difficult to achieve for maximum productivity [20
Domestication of other non-legume perennial grains is already underway for perennial rice (Oryza
], perennial wheat (Triticum
], Sorghum (Sorghum
] and Silphium integrifolium
]. Some tropical perennial grain legumes already exist and are being grown either commercially or in subsistence settings, such as pigeon pea (Cajanus cajan
]. Less research has been accomplished and is actively ongoing in breeding and developing a perennial grain legume adapted to temperate climates except for some work involving Illinois bundleflower in the US [28
] and a screen of potential candidate perennial grain legumes for Australian cropping systems [30
Past efforts to breed and domesticate other perennial grains have generated hypotheses about why annual grains were historically domesticated instead of perennial grains [32
] and provided evidence suggesting how current knowledge about the ecology of perennial plants and ecosystems, combined with modern breeding approaches, makes domestication of perennial grains now possible [16
]. Researchers from The Land Institute (Salina, KS, USA) and elsewhere have outlined a pipeline strategy as a guide for grain crop domestication which is composed of three phases (Phase I: Evaluating candidate species; Phase II: Wild species to new crop; and Phase III: From new crop to commodity crop) [34
]. Earlier approaches propose candidate screening and selection by determining mean values for desirable traits from a single study or via species-centric approaches that attempt to identify purpose for a promising plant. Instead, the pipeline domestication model attempts to monitor multiple species’ abilities to meet a predefined purpose through multiple phases of selection designed to overcome the limitations that exist for each species [34
]. Phase I: Evaluating candidate species, closely resembles a screen for desirable traits or attributes that fit a predefined agricultural target, but more importantly, Phase I aims to identify the primary limitations of each species and to develop specific breeding strategies to address those limitations in Phase II.
Perennial grain legumes are entering Phase I of the pipeline, and the remainder of this review aims to use the ideas developed in the pipeline strategy to outline legume-specific morphological traits or ecophysiological attributes that we assume are desirable for an herbaceous, perennial, temperate-adapted grain legume that is mechanically harvested on a commercial scale. In doing so, we provide relevant data collected for a small group of perennial herbaceous legume species related to the described attributes and suggest a few strategies for evaluating and selecting candidate species to move forward to Phase II of the pipeline.
The criteria developed and presented herein are provided as a guide for ranking and screening species with the potential to become temperate-adapted, herbaceous perennial grain legumes suitable for mechanical harvest within commercial agriculture. Because plant domestication efforts should be initiated with a particular agricultural target in mind [34
], some of the criteria may not be relevant for other agricultural settings (subsistence, tropical, and/or intercrop cropping systems that have commonly included trailing and vining grain legume species) even though they may be equally in need of new perennial grain legume species. Likewise, the few dozen species presented here within tables are not intended to represent the most promising or only species that merit initial consideration and evaluation, rather they serve as an example of how data for many of the criteria to be used in Phase I of the domestication pipeline can be acquired for some legumes using species monographs, looking at herbarium specimens and reading peer-reviewed literature. However, the size of the Fabaceae (more than 19,500 species) and its broad distribution across continents suggests that there are still many other potential candidates whose attributes are unknown and unavailable because they lacked previous agricultural interest or because their native regions have been underexplored.
Until recently, it was not even clear how many of the Fabaceae were herbaceous and perennial species, primary criteria for perennial grain legume candidates. To this end, a novel partnership uniting plant breeders, ethnobotanists and plant evolutionary biologists from The Land Institute, the Missouri Botanical Garden and Saint Louis University has been established to conduct a global inventory of perennial, herbaceous members of the Fabaceae, Asteraceae and Poaceae (Perennial Agriculture Project Global Inventory (PAPGI)). This ongoing project is intended to bridge knowledge gaps between botanical and agricultural research communities by compiling information originally collected by botanists for taxonomic, systematics and ethnobotanical purposes and making it accessible to breeders working to develop perennial grain crops through an online, searchable database (Ciotir et al., unpublished). Ultimately, the PAPGI will expand upon the work done here, offering an extensive accessible knowledge framework to support the development of novel, perennial grain crops from wild, previously undomesticated plant species for a wide variety of cropping systems and agricultural settings.
Lastly, Phase I of the pipeline strategy is not meant to be an exercise in simply gathering data about certain traits for potential species through database searches or empirical research; rather, it is also intended to be an evaluation that ranks and identifies species most likely to be successfully domesticated and grown as a crop. While surveys of important attributes can help narrow the list, previously unforeseen limitations and opportunities are likely to be revealed by simply planting, growing and harvesting seed from the candidates within agricultural settings [26
]. Furthermore, because no species is expected to have all or even a handful of the required attributes, the time required to acquire the necessary traits or overcome known limitations via breeding is also unforeseeable. Breeding populations must be developed and selection must be performed for each species to identify heritable variation for crucial domestication traits, estimate response to selection for the traits and predict the rates of genetic gain (the domestication timeline) that can be expected. Therefore, only by growing the species and performing simple selection experiments can final decisions be made about which domesticates to drop from the pipeline and which to move forward to Phase II: Wild Species to New Crop. This approach represents a largely unexplored and rewarding area of potential research for breeders, evolutionary biologists and classical botanists alike.