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Sci Rep. 2020 Feb 25;10(1):3416. doi: 10.1038/s41598-020-60166-4.

Evaluation of pulse crops' functional diversity supporting food production.

Scientific reports

Julie Guiguitant, Denis Vile, Michel Edmond Ghanem, Jacques Wery, Hélène Marrou

Affiliations

  1. Montpellier SupAgro, INRAE, CIRAD, IAMM, Univ Montpellier, SYSTEM, F-34060, Montpellier, France.
  2. INRAE, Montpellier SupAgro, Univ Montpellier, LEPSE, F-34060, Montpellier, France.
  3. INRAE, Montpellier SupAgro, Univ Montpellier, LEPSE, F-34060, Montpellier, France. [email protected].
  4. University Mohammed VI Polytechnic, AgroBioSciences, Benguerir, Morocco.
  5. International Center for Agricultural Research in the Dry Areas (ICARDA), Cairo, Egypt.
  6. University Mohammed VI Polytechnic, AgroBioSciences, Benguerir, Morocco. [email protected].
  7. Montpellier SupAgro, Univ Montpellier, F-34060, Montpellier, France. [email protected].

PMID: 32098982 PMCID: PMC7042262 DOI: 10.1038/s41598-020-60166-4

Abstract

Pulses, defined as legumes which produce dry seed used for human consumption, are plants of great agronomic value, at the food system level as much as the field level but their diversity has been largely underused. This study aimed at analyzing existing data on cultivated pulse species in the literature to provide a broad and structured description of pulses' interspecific functional diversity. We used a functional trait-based approach to evaluate how pulse diversity could support food production in agroecosystems constrained by low water and nutrient availability and exposed to high weed pressure. We gathered data for 17 functional traits and six agroecosystem properties for 43 pulse species. Our analytical framework highlights the correlations and combinations of functional traits that best predict values of six agroecosystem properties defined as ecosystem services estimates. We show that pulse diversity has been structured both by breeding and by an environmental gradient. The covariance space corresponding to agroecosystem properties was structured by three properties: producers, competitors, stress-tolerant species. The distribution of crop species in this functional space reflected ecological adaptive strategies described in wild species, where the size-related axis of variation is separated from variation of leaf morpho-physiological traits. Six agroecosystem properties were predicted by different combinations of traits. However, we identified ubiquitous plant traits such as leaflet length, days to maturity, seed weight, and leaf nitrogen content, that discriminated agroecosystem properties and allowed us to gather individual species into three clusters, representative of the three strategies highlighted earlier. Implications for pulses provisioning of services in agroecosystems are discussed.

References

  1. Singh, B. B., Ajeigbe, H. A., Tarawali, S. A., Fernandez-Rivera, S. & Abubakar, M. Improving the production and utilization of cowpea as food and fodder. Field Crops Res. 84, 169–177 (2003). - PubMed
  2. Tharanathan, R. N. & Mahadevamma, S. Grain legumes - A boon to human nutrition. Trends Food Sci. Technol. 14, 507–518 (2003). - PubMed
  3. Stagnari, F., Maggio, A., Galieni, A. & Pisante, M. Multiple benefits of legumes for agriculture sustainability: an overview. Chem. Biol. Technol. Agric. 4, 2 (2017). - PubMed
  4. Edwards, T. J. Legumes of the World. South Afr. J. Bot. 73, 272–273 (2007). - PubMed
  5. Doyle, J. J. The Rest of the Iceberg. Legume Diversity and Evolution in a Phylogenetic Context. Plant Physiol. 131, 900–910 (2003). - PubMed
  6. De Boer, J. & Aiking, H. Prospects for pro-environmental protein consumption in Europe: Cultural, culinary, economic and psychological factors. Appetite 121, 29–40 (2018). - PubMed
  7. Cuevas, J. A. Neglected Crops 1942 from a different perspective. https://doi.org/10.1017/CBO9781107415324.004 (1992). - PubMed
  8. Foyer, C. H. et al. Neglecting legumes has compromised human health and sustainable food production. Nat. Plants 2, 16112 (2016). - PubMed
  9. Padulosi, S., Thompson, J. & Rudebjer, P. Neglected and underutilized species (2013). - PubMed
  10. Tiwari, B. K., Gowen, A. & McKenna, B. M. Pulse foods: processing, quality and nutraceutical applications. (Academic Press, 2011). - PubMed
  11. Padulosi, S., Eyzaquirre, P. & Hodgkin, T. Challenges and strategies in promoting conservation and use of neglected and underutilized crop species. Perspect. New Crops New Uses 140–140, https://doi.org/10.1016/j.ajem.2008.02.004 (1999). - PubMed
  12. Ghane, S. G., Lokhande, V. H., Ahire, M. L. & Nikam, T. D. Indigofera glandulosa Wendl. (Barbada) a potential source of nutritious food: Underutilized and neglected legume in India. Genet. Resour. Crop Evol. 57, 147–153 (2010). - PubMed
  13. Mal, B. Neglected and underutilized crop genetic resources for sustainable agriculture. Indian J. Plant Genet. Resour. 20, 1–14 (2007). - PubMed
  14. Dansi, A. et al. Diversity of the neglected and underutilized crop species of importance in benin. Sci. World J. 2012 (2012). - PubMed
  15. Magrini, M.-B. et al. Why are grain-legumes rarely present in cropping systems despite their environmental and nutritional benefits? Analyzing lock-in in the French agrifood system. Ecol. Econ. 126, 152–162 (2016). - PubMed
  16. Massawe, F., Mayes, S. & Cheng, A. Crop diversity: an unexploited treasure trove for food security. Trends Plant Sci. 21, 365–368 (2016). - PubMed
  17. Drewnowski, A. Healthy diets for a healthy planet. Am. J. Clin. Nutr. 99, 1284–1285 (2014). - PubMed
  18. Ebert, A. W. Potential of Underutilized Traditional Vegetables and Legume Crops to Contribute to Food and Nutritional Security, Income and More Sustainable Production Systems. Sustainability 6, 319–335 (2014). - PubMed
  19. Tilman, D. et al. Diversity and productivity in a long-term grassland experiment. Science 294, 843–846 (2001). - PubMed
  20. Jackson, L. E., Pascual, U. & Hodgkin, T. Utilizing and conserving agrobiodiversity in agricultural landscapes. Agric. Ecosyst. Environ. 121, 196–210 (2007). - PubMed
  21. Garnier, E. & Navas, M. L. A trait-based approach to comparative functional plant ecology: concepts, methods and applications for agroecology. Agron. Sustain. Dev. 32, 365–399 (2012). - PubMed
  22. Martin, A. R. & Isaac, M. E. Plant functional traits in agroecosystems: A blueprint for research. Journal of Applied Ecology 52, 1425–1435 (2015). - PubMed
  23. Wood, S. A. et al. Functional traits in agriculture: Agrobiodiversity and ecosystem services. Trends Ecol. Evol. 30, 531–539 (2015). - PubMed
  24. Lavorel, S. & Garnier, E. Predicting changes in community composition and ecosystem functioning from plant traits: Revisiting the Holy Grail. Functional Ecology 16, 545–556 (2002). - PubMed
  25. Garnier, E. et al. Assessing the effects of land-use change on plant traits, communities and ecosystem functioning in grasslands: A standardized methodology and lessons from an application to 11 European sites. Ann. Bot. 99, 967–985 (2007). - PubMed
  26. Violle, C. et al. Let the concept of trait be functional! Oikos 116, 882–892 (2007). - PubMed
  27. Cordier, M., Pérez Agúndez, J. A., Hecq, W. & Hamaide, B. A guiding framework for ecosystem services monetization in ecological–economic modeling. Ecosyst. Serv. 8, 86–96 (2014). - PubMed
  28. Jordan, S. J. et al. Ecosystem services altered by human changes in the nitrogen cycle: a new perspective for US decision making. Ecol. Lett. 14, 804–815 (2011). - PubMed
  29. Grime, J. P. et al. Integrated screening validates priary axes of specialisation in plants. Oikos 79, 259–281 (1997). - PubMed
  30. Grime, J. P. Primary strategies in plants. Trans. Bot. Soc. Edinb. 43, 151–160 (2009). - PubMed
  31. Pierce, S. et al. A global method for calculating plant CSR ecological strategies applied across biomes world‐wide. Funct. Ecol. 31, 444–457 (2017). - PubMed
  32. Yousfi, N., Slama, I., Ghnaya, T., Savouré, A. & Abdelly, C. Effects of water deficit stress on growth, water relations and osmolyte accumulation in Medicago truncatula and M. laciniata populations. Comptes Rendus - Biol. 333, 205–213 (2010). - PubMed
  33. Norman, H. C., Cocks, P. S. & Galwey, N. W. Hardseededness in annual clovers: variation between populations from wet and dry environments. Aust. J. Agric. Res. 53, 821–821 (2002). - PubMed
  34. Berger, J. D., Shrestha, D. & Ludwig, C. Reproductive strategies in mediterranean legumes: trade-offs between phenology, seed size and vigor within and between wild and domesticated Lupinus species collected along aridity gradients. Front. Plant Sci. 8, 548–548 (2017). - PubMed
  35. Berger, J. D. & Ludwig, C. Contrasting adaptive strategies to terminal drought-stress gradients in Mediterranean legumes: phenology, productivity, and water relations in wild and domesticated Lupinus luteus L. J. Exp. Bot. 65, 6219–6229 (2014). - PubMed
  36. Westoby, M. A leaf-height-seed (LHS) plant ecology strategy scheme. Plant Soil 199, 213–227 (1998). - PubMed
  37. Moles, A. T., Falster, D. S., Westoby, M., Wright, I. J. & Vesk, P. A. Plant ecological strategies: some leading dimensions of variation between species. Annu. Rev. Ecol. Syst. 33, 125–159 (2002). - PubMed
  38. Quétier, F., Lavorel, S., Thuiller, W. & Davies, I. Plant-trait-based modeling assessment of ecosystem-service sensitivity to land-use change. Ecol. Appl. 17, 2377–2386 (2007). - PubMed
  39. Saugier, B. Plant strategies, vegetation processes, and ecosystem properties. Plant Sci. 161, 813–813 (2001). - PubMed
  40. Lavergne, S., Garnier, E. & Debussche, M. Do rock endemic and widespread plant species differ under the Leaf-Height-Seed plant ecology strategy scheme? Ecol. Lett. 6, 398–404 (2003). - PubMed
  41. Gaudet, C. L. & Keddy, P. A. A comparative approach to predicting competitive ability from plant traits. Nature 334, 242–243 (1988). - PubMed
  42. Hodgson, A. J. G., Wilson, P. J., Hunt, R., Grime, J. P. & Thompson, K. Allocating C-S-R plant functional types: a soft approach to a hard problem. Oikos 85, 282–294 (1999). - PubMed
  43. Willson, M. F. Dispersal mode, seed shadows, and colonization patterns. in Frugivory and seed dispersal: ecological and evolutionary aspects (eds. Fleming, T. H. & Estrada, A.) 261–280, https://doi.org/10.1007/978-94-011-1749-4_19 .(Springer Netherlands, 1993). - PubMed
  44. Askew, A. P., Corker, D., Hodkinson, D. J. & Thompson, K. A New Apparatus to Measure the Rate of Fall of Seeds. Funct. Ecol. 11, 121–125 (1997). - PubMed
  45. Cipollini, M. L. & Stiles, E. W. Seed predation by the bean weevil acanthoscelides obtectus on phaseolus species: consequences for seed size, early growth and reproduction. Oikos 60, 205–214 (1991). - PubMed
  46. Leishman, M. R., Wright, I. J., Moles, A. T. & Westoby, M. The evolutionary ecology of seed size. In Seeds: The Ecology of Regeneration in Plant Communities 31–57, https://doi.org/10.1086/284440 (1985). - PubMed
  47. Volaire, F. A unified framework of plant adaptive strategies to drought: Crossing scales and disciplines. Glob. Change Biol. 24, 2929–2938 (2018). - PubMed
  48. Wright, I. J. et al. The worldwide leaf economics spectrum. Nature 428, 821–7 (2004). - PubMed
  49. Díaz, S. et al. The global spectrum of plant form and function. Nature 529, 167–171 (2016). - PubMed
  50. Lambers, H. & Poorter, H. Inherent variation in growth rate between higher plants: a search for physiological causes and ecological consequences. Adv. Ecol. Res. 23, 187–261 (1992). - PubMed
  51. Poorter, H. & Remkes, C. Leaf area ratio and net assimilation rate of 24 wild species differing in relative growth rate. Plant Ecol. 553–559 (1990). - PubMed
  52. Poorter, H., Niinemets, U., Poorter, L., Wright, I. J. & Villar, R. Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytol. 182, 565–588 (2009). - PubMed
  53. Tribouillois, H., Cruz, P., Cohan, J.-P. & Justes, É. Modelling agroecosystem nitrogen functions provided by cover crop species in bispecific mixtures using functional traits and environmental factors. Agric. Ecosyst. Environ. 207, 218–228 (2015). - PubMed
  54. Borrell, A. K. & Hammer, G. L. Nitrogen dynamics and the physiological basis of stay-green in Sorghum. Crop Sci. 40, 1295–1307 (2000). - PubMed
  55. Chapin, S. F. 16 - Functional role of growth forms in ecosystem and global processes. in Scaling Physiological Processes (eds. Ehleringer, J. R. & Field, C. B.) 287–312, https://doi.org/10.1016/B978-0-12-233440-5.50024-5 (Academic Press, 1993). - PubMed
  56. Ta, C. T. & Weiland, R. T. Nitrogen partitioning in Maize during early development. Crop Sci. 32, 443–443 (2010). - PubMed
  57. Borrell, A., Hammer, G. & Van Oosterom, E. Stay-green: A consequence of the balance between supply and demand for nitrogen during grain filling? Ann. Appl. Biol. 138, 91–95 (2001). - PubMed
  58. Reich, P. B., Walters, M. B. & Ellsworth, D. S. From tropics to tundra: global convergence in plant functioning. Proc. Natl. Acad. Sci. USA 94, 13730–4 (1997). - PubMed
  59. Kikuzawa, K. A cost-benefit analysis of leaf habit and leaf longevity of trees and their geographical pattern. Am. Nat. 138, 1250–1263 (1991). - PubMed
  60. Fayaud, B., Coste, F., Corre-Hellou, G., Gardarin, A. & Dürr, C. Modelling early growth under different sowing conditions: A tool to predict variations in intercrop early stages. Eur. J. Agron. 52, 180–190 (2014). - PubMed
  61. Tamet, V., Boiffin, J., Dürr, C. & Souty, N. Emergence and early growth of an epigeal seedling (Daucus carota L.): Influence of soil temperature, sowing depth, soil crusting and seed weight. Soil Tillage Res. 40, 25–38 (1996). - PubMed
  62. Chapin, F. S., Autumn, K. & Pugnaire, F. Evolution of suites of traits in response to environmental stress. Am. Nat. 142, S78–S92 (2002). - PubMed
  63. Smartt, J. The evolution of pulse crops. Econ. Bot. 32, 185–198 (1978). - PubMed
  64. Plaza-Bonilla, D., Nolot, J.-M., Raffaillac, D. & Justes, E. Innovative cropping systems to reduce N inputs and maintain wheat yields by inserting grain legumes and cover crops in southwestern France. Eur. J. Agron. 82, 331–341 (2017). - PubMed
  65. Nambiar, P. T. C., Rupela, O. P. & Kumar Rao, J. V. D. K. Nodulation and nitrogen fixation in groundnut (Arachis hypogaea L.), chickpea (Cicer arietinum L.) and pigeonpea (Cajanus cajan L. millsp.). Biol. Nitrogen Fixat. Recent Dev. Ed. NS Subba Rao (1988). - PubMed
  66. Hardarson, G. et al. Genotypic variation in biological nitrogen fixation by common bean. Plant Soil 152, 59–70 (1993). - PubMed
  67. Reichardt, K., Hardarson, G., Zapata, F., Kirda, C. & Danso, S. K. A. Site Variability effect on field measurement of symbiotic nitrogen fixation using the 15N isotope dilution method. Soil Biol. Biochem. 19, 405–409 (1987). - PubMed
  68. Piha, M. I. & Munns, D. N. Nitrogen fixation capacity of field-grown bean compared to other grain legumes. Agron. J. 79, 690–696 (1987). - PubMed
  69. Kumar Rao, J. V. D. K. & Dart, P. J. Nodulation, nitrogen fixation and nitrogen uptake in pigeonpea (Cajanus cajan (L.) Millsp) of different maturity groups. Plant Soil 99, 255–266 (1987). - PubMed
  70. Vance, C. P. Legume symbiotic nitrogen fixation: Agronomic aspects. The Rhizobiaceae 509–530, https://doi.org/10.1007/978-94-011-5060-6_26 . (2011). - PubMed
  71. McKey, D. Legumes and nitrogen: The evolutionary ecology of a nitrogen-demanding lifestyle. Adv. Legume Syst. 5 Nitrogen Factor 5, 211–228 (1994). - PubMed
  72. Leavitt, J. R. C., Dobrenz, A. K. & Stone, J. E. Physiological and morphological characteristics of large and small leaflet alfalfa genotypes. Agron. J. 71, 529–529 (1979). - PubMed
  73. Schubert, K. R. Enzymes of purine biosynthesis and catabolism in Glycine max. 1115–1122 (1981). - PubMed
  74. Herridge, D. F. & Pate, J. S. Utilization of net photosynthate for nitrogen fixation and protein Production in an annual legume. Plant Physiol. 60, 759–764 (2008). - PubMed
  75. Tissue, D. T., Megonigal, J. P. & Thomas, R. B. Nitrogenase activity and N2 fixation are stimulated by elevated CO2 in a tropical N2-fixing tree. Oecologia 109, 28–33 (1997). - PubMed
  76. Hartwig, U. A., Lüscher, A., Nösberger, J. & Van Kessel, C. Nitrogen-15 budget in model ecosystems of white clover and perennial ryegrass exposed for four years at elevated atmospheric pCO2. Glob. Change Biol. 8, 194–202 (2002). - PubMed
  77. Hartwig, U. A. The regulation of symbiotic N2 fixation: a conceptual model of N feedback from the ecosystem to the gene expression level. Perspect. Plant Ecol. Evol. Syst. 1, 92–120 (1998). - PubMed
  78. Poorter, H. Construction costs and payback time of biomass: a whole plant perspective. Whole Plant Perspect. Carbon-Nitrogen Interact. 111–127 (1994). - PubMed
  79. Kruidhof, H. M., Bastiaans, L. & Kropff, M. J. Ecological weed management by cover cropping: Effects on weed growth in autumn and weed establishment in spring. Weed Res. 48, 492–502 (2008). - PubMed
  80. Fan, F. et al. Nitrogen fixation of faba bean (Vicia faba L.) interacting with a non-legume in two contrasting intercropping systems. Plant Soil 283, 275–286 (2006). - PubMed
  81. Craine, J. M. & Dybzinski, R. Mechanisms of plant competition for nutrients, water and light. Funct. Ecol. 27, 833–840 (2013). - PubMed
  82. Corre-Hellou, G., Fustec, J. & Crozat, Y. Interspecific competition for soil N and its interaction with N2 fixation, leaf expansion and crop growth in pea-barley intercrops. Plant Soil 282, 195–208 (2006). - PubMed
  83. Nesheim, L. & Boller, B. C. Nitrogen fixation by white clover when competing with grasses at moderately low temperatures. Plant Soil 133, 47–56 (1991). - PubMed
  84. Bedoussac, L. & Justes, E. Dynamic analysis of competition and complementarity for light and N use to understand the yield and the protein content of a durum wheat-winter pea intercrop. Plant Soil 330, 37–54 (2010). - PubMed
  85. Alege, G. O., Abu, N. E. & Sunday, C. E. Seed protein electrophoresis of some members of the family fabaceae. Afr. J. Biotechnol. 13, 3730–3735 (2014). - PubMed
  86. Kazakou, E. et al. Are trait‐based species rankings consistent across data sets and spatial scales? J. Veg. Sci. 25, 235–247 (2014). - PubMed
  87. Tipping, M. E. & Bishop, C. M. Probabilistic principal component analysis. J R Statisit Soc B 61, 611–622 (1999). - PubMed
  88. Breiman, L., Friedman, J., Stone, C. J. & Olshen, R. A. Classification and regression trees. (Chapman & Hall, 1994). - PubMed
  89. R Core Team. R: The R project for statistical computing (2018). - PubMed
  90. Stacklies, W., Redestig, H., Scholz, M., Walther, D. & Selbig, J. pcaMethods a bioconductor package providing PCA methods for incomplete data. Bioinformatics 23, 1164–1167 (2007). - PubMed
  91. Therneau, T., Atkinson, B., Ripley, B. & Ripley, M. B. rpart: recursive partitioning and regression trees. R Package Version 41–10 (2015). - PubMed

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