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2022 Volume 2
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REVIEW   Open Access    

Mining and utilization of salinity tolerant legumes in tropical coastal agroecosystems: An overview

  • # These authors contributed equally: Yiming Liu, Mary Atieno

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  • Received Date: 18 September 2022
    Accepted Date: 16 November 2022
    Published Online: 21 December 2022
    Grass Research  2 Article number: 10 (2022)  |  Cite this article
  • Coastal saline soils are increasing year by year caused by climate change and human activities. Most of the coastal saline soils are idle due to their high salinity level and few crops can grow normally. Salinity tolerant legumes are naturally tolerant to salt, which can ecologically cover the coastal saline soil, enhance soil fertility by symbiotic nitrogen fixation and increase the smallholder farmers’ benefits in terms of forage, green manure, food or medicine. However, few reports are available for the systematic evaluation of salinity tolerant legumes. This review summarizes and evaluates currently available salinity tolerant legume species that could potentially be used and discusses their potential for integration into smallholder mixed coastal systems of the Asia-Pacific region. Fourty four salinity tolerant legumes were summarized, six of them showed a high level of salinity tolerance, 17 of them showed a moderate level of salinity tolerance and 21 of them showed potential salinity tolerance but need to be further studied. Many gaps such as combined tolerance evaluation, nitrogen fixation efficiency, animal feeding experiments and salinity tolerant rhizobia screening/inoculants exist. Case studies demonstrate legumes could be used to reclaim coastal saline soils, but commitment and support from government and public services are necessary to address both seed system and extension needs, through the provision of adequate incentives, policies and development efforts.
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  • Cite this article

    Liu Y, Atieno M, Cardoso JA, Yang H, Xu Bin, et al. 2022. Mining and utilization of salinity tolerant legumes in tropical coastal agroecosystems: An overview. Grass Research 2:10 doi: 10.48130/GR-2022-0010
    Liu Y, Atieno M, Cardoso JA, Yang H, Xu Bin, et al. 2022. Mining and utilization of salinity tolerant legumes in tropical coastal agroecosystems: An overview. Grass Research 2:10 doi: 10.48130/GR-2022-0010

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Mining and utilization of salinity tolerant legumes in tropical coastal agroecosystems: An overview

Grass Research  2 Article number: 10  (2022)  |  Cite this article

Abstract: Coastal saline soils are increasing year by year caused by climate change and human activities. Most of the coastal saline soils are idle due to their high salinity level and few crops can grow normally. Salinity tolerant legumes are naturally tolerant to salt, which can ecologically cover the coastal saline soil, enhance soil fertility by symbiotic nitrogen fixation and increase the smallholder farmers’ benefits in terms of forage, green manure, food or medicine. However, few reports are available for the systematic evaluation of salinity tolerant legumes. This review summarizes and evaluates currently available salinity tolerant legume species that could potentially be used and discusses their potential for integration into smallholder mixed coastal systems of the Asia-Pacific region. Fourty four salinity tolerant legumes were summarized, six of them showed a high level of salinity tolerance, 17 of them showed a moderate level of salinity tolerance and 21 of them showed potential salinity tolerance but need to be further studied. Many gaps such as combined tolerance evaluation, nitrogen fixation efficiency, animal feeding experiments and salinity tolerant rhizobia screening/inoculants exist. Case studies demonstrate legumes could be used to reclaim coastal saline soils, but commitment and support from government and public services are necessary to address both seed system and extension needs, through the provision of adequate incentives, policies and development efforts.

    • The rising sea-levels caused by global warming poses a major threat to coastal regions due to salt-water intrusion and damage to agricultural land[1]. Over the past 20 years, the sea level has risen by about 8 cm[2]. Based on a new digital elevation model (CoastalDEM) utilizing neural networks, Kulp & Strauss found that the rising sea levels and coastal flooding have tripled as compared to the previous estimate by Shuttle Radar Topography Mission (SRTM)[3]. About 1 billion people occupy land lying less than 10 m above current high tide lines, most of them living in the Asia and Pacific region, mainly in China, Bangladesh, India, Vietnam, Indonesia, Thailand, Philippines and Japan[3]. The latest global soil salinity map of 2016 showed that the total area of salt affected land is around 1 billion hectares, an increase of more than 100 Mha from 1986[4]. Tidal flats occupy an area of about 124,286−131,821 km2 globally, with about 11.27% in Indonesia, 9.42% in China, 6.93% in Australia, 4.52% in India and 2.59% in Myanmar[5].

      Increased area of saline soils including large areas of tidal flats have significant impacts on the natural environment and ecosystems as well as socio-economic impacts[6]. High salinity levels in the soil harm plant growth and limit crop yields. Currently, most of the salt-affected soils, especially coastal saline soils, have been deserted by many farmers leaving extensive areas of idle and unproductive land. This has posed a big challenge to researchers and farmers on how best to fully utilize these saline areas.

      Among the various techniques to reclaim saline soil, phytoremediation is generally preferred compared to e.g. hydro or electro reclamation as it is sustainable and economically viable[7]. Phytoremediation involves the use of plants and associated soil micro-organisms to reduce the harmful effects of contaminants in the environment[8,9]. For instance, legumes make net nitrogen inputs into ecosystems, and have other multiple environmental benefits by improving soil structure and microbial activity of coastal saline land, and fundamentally improve saline soil[10]. Salinity tolerant legumes offer the double advantage of reclaiming degraded coastal agroecosystems and providing a local source of livestock feed. The latter is particularly relevant in highly populated countries mainly depending on feed imports, which is often the case in the Asia-Pacific region[11]. In terms of livestock feed, salinity tolerant legumes improve the quantity and quality of available feed, and have a high nutritional value with high protein content. When grown in areas that are not suitable for crops, they allow farmers to make the most of available land, provide increased income and diversify livelihoods of coastal farmers[12].

      Salinity tolerant legumes grow naturally in many coastal countries, and are receiving increasing attention from researchers and developers due to their adaptation capacities in a range of salinity and drought conditions, and their potential economic benefits[13,14]. Fully mining and using these plants to improve coastal saline areas and tidal flats is an effective means to overcome impacts of seawater encroachment and increase the livelihoods of 1 billion coastal smallhold farmers[3].

      However, there has been no attempt so far to synthesize knowledge on salinity tolerant legumes and promote their use in coastal ecosystems. Collections and selections have been scattered, mainly in Colombia, China, Australia, India etc.[15,16]. International Center for Tropical Agriculture (CIAT) (www.tropicalforages.info/text/intro/index.html), Chinese Academy of Tropical Agricultural Sciences (CATAS)[17], Commonwealth Scientific and Industrial Research Organization (CSIRO) and The International Livestock Research Institute (ILRI) have engaged in the collection and preservation of forage germplasm resources from 1970[18], but the quantity of salinity tolerant legumes are still low. There is an urgent need to systematically review available coastal forage legume plant resources in order to provide theoretical guidelines for the improvement of coastal saline land. Therefore, the objectives of this study were to (i) review currently available salinity tolerant forage legume species, (ii) discuss their potential for integration into smallholder mixed coastal systems of the Asia-Pacific region, and (iii) present the most promising species in more detail.

    • Great breakthroughs have been made in the research on the mechanism of plant salinity tolerance, mainly focusing on model plants Arabidopsis thaliana and crops[19]. It's clear that salinity tolerance mechanisms of plants are complex traits involving multiple phases and genes[20]. At the cellular level, salinity tolerant plants maintain this ion balance by excreting Na+ out of the cell or compartmentalizing Na+ into the vacuole and accumulate osmolytes (such as K+, Ca2+, proline, soluble sugar, polyamines etc.) in the cytoplasm. Glycosyl inositol phosphorylceramide (GIPC) sphingolipids in the plasma membrane act as Na+ receptors for sensing Na+ in the apoplastic space and then gate Ca2+ influx channels in plants[21]. With the increase of Ca2+, the salt overly sensitive (SOS) signaling pathways (SOS1, SOS2, SOS3) will be activated and play a leading role in mediating the excretion of Na+ in plants[19]. Many other pathways such as MAPK and salinity tolerance related genes (including transcription factors) will also be activated to deal with salinity stress through osmoregulation, ion transport and radical-scavenging. At the tissue or organ level, some salinity tolerant plants usually store Na+ in the roots instead of above ground, or old leaves instead of young leaves[22].

      For the salinity tolerant legumes, many of them are belonging to halophytes (plants that survive to complete their life cycle in at least 200 mM salinity)[2325], besides the common salinity tolerant mechanisms similar to Arabidopsis thaliana and crops, many of them have special salinity tolerant mechanisms due to their different morphological structure[26]. Big gaps on the study of salinity tolerant mechanisms based on the whole genome sequencing and lack of studies about the function of special salinity tolerant genes.

    • Rhizobia is a special group of microbes with the unique ability to form symbiotic association with legumes to fix atmospheric nitrogen, a process known as Biological Nitrogen Fixation (BNF)[27]. Rhizobia-legume association takes place in specialized root structures called nodules, where rhizobia convert atmospheric gaseous dinitrogen (N2) into ammonia, a form that can be assimilated by the plants; in exchange, the host plant provides carbon compounds to rhizobia[2830] . For centuries, this symbiotic association has been used in cropping systems as the most important N-fixing agent[31,32].

      Salt stress can inhibit rhizobia-legume symbiosis by reducing rhizobia growth, nodule formation and BNF due to osmotic stress and high toxic levels of Na+ and Cl- in the cells[33]. Different rhizobia species exhibit varying levels of tolerance to salt stress. Fast-growing rhizobia species are categorized as more salinity-tolerant e.g. Sinorhizobium meliloti[34], S. fredii[35], Mesorhizobium huakuii and Rhizobium tropici[36] as compared to slow-growing rhizobia such as R. leguminosarum bv. viciae[37]. Some rhizobia strains have one or several high tolerant abilities to abiotic stress such as high temperature, pH, salinity and drought[38].

      Previous studies have reported rhizobia to be more tolerant to salinity as compared to the host legumes plants, and can enhance tolerance of legumes to salt stress and yield[3941]. Salinity-adaptive responses in rhizobia include accumulation of osmoprotectants, enhanced production of exopolysaccharides, expression of stress genes and ROS-scavenging enzymes such as superoxide dismutase[42,43]. Intracellular accumulation of osmoprotectants such as glycine betaine, glutamate, choline and N-acetyl glutaminyl glutamine amide (NAGGN) have been correlated with salt stress tolerance in Rhizobium meliloti[44,45]. Salinity tolerance of rhizobia is also related to hormones and protein changes. For example, increased salinity tolerance of Bradyrhizobium strain RJS9-2 may be achieved by production of indole-3-acetic acid (IAA), protein expression and osmoprotectant accumulation[46]. Salinity tolerant rhizobia may be due to a plasmid-mediated resistance since salinity resistance can be rapidly transferred from tolerant to sensitive rhizobia[38].

      Biofertilizers containing rhizobia are an environmentally friendly approach to enhance soil fertility and legume productivity. Establishment of salinity-tolerant legumes combined with inoculation using salinity-tolerant rhizobia strains is a promising strategy for forage legume production and reclamation of saline soils. Generally, farmers can purchase commercial rhizobia inoculants to apply to the legumes. However, most countries in Asia rely on imported biofertilizers as only few rhizobia inoculants are registered or available in the market, the majority being of poor quality. For instance, by 2018, only 1% of biofertilizers/inoculants registered in China contained rhizobia, mainly produced for Chinese milkvetch (Astragalus sinicus), soybean and peanuts[33]. In Vietnam, there are very few rhizobia inoculants available in the market[47], while in Cambodia and Lao PDR, low availability and adoption of rhizobia inoculants have been reported[33]. This shows a gap and a huge need to develop and promote the use of rhizobia inoculants including salinity-tolerant rhizobia inoculants in this context. Selection of high salinity tolerant legumes and the application of legume-specific, high salinity tolerant rhizobia inoculants has immense potential for successful rhizobium-legume symbiosis and increased N inputs in saline soils.

    • The current known salinity tolerant forage legume species and potentially salinity tolerant species in the tropical regions are summarized in Table 1. Only one species Melilotus indicus (L.) All. is an annual plant, five species are annual or perennial plants, 38 species are perennial plants. Twenty five percent of the 44 species are shrubs, 52% of the 44 species are herbs, 6.8% of the 44 species are trees, the rest have more than one growth habit. No variety was available in the 21 species (47.7% of the total species), indicate that breeding of salinity tolerant legumes needs to be strengthened in the future (Table 1).

      Table 1.  General information of current salinity tolerant forage legume species.

      No.Scientific nameCommon nameVarietyDistribution*Life cycleGrowth habit
      1Abrus precatorius L.Rosary peaTropical zonesPerennialShrub
      2Acacia dealbata LinkMimosaDealbata Link, 1846; Mackayana Seem.World widePerennialShrub or tree
      3Acacia nilotica (L.) Willd. ex DelileGum arabic treecupressiformisAfricaPerennialTree
      4Alysicarpus vaginalis (L.) DC.Alyce Clover, Buffalo cloveNummularifolius (DC.) Miq., Parvifolius Verdc., stocksii Baker taiwanianus S.S. Ying, Vaginalis, venosa (Blat.& Hall.) A. Pramanik & Thoth.Tropical zonesPerennialHerb
      5Arachis pintoi Krapov. & W.C.Greg.Pinto PeanutBelomonte, Reyan No.12Tropical zones of South AmericaPerennialHerb
      6Cajanus cajan (L.) Millsp.Pigeon pea, gungo peaPhule Tur-12, Babati White, bicolor DC., Cajan, flavus DC.Tropical zonesPerennialShrub
      7Calopogonium mucunoides Desv.Calopo, wild ground nutTropical zonesPerennialHerb
      8Canavalia ensifomis (L.) DCJack bean, horse beanCoriacea Domin, Ensiformis, Normalis KuntzeTropical zonesPerennialHerbaceous vine
      9Canavalia rosea (Sw.) DC.Bay beanTropical zonesPerennialHerbaceous vine
      10Cassia pumila Lam.Tropical zones in China, India, Malaysia and AustraliaPerennialShrub
      11Centrosema pubescens Benth.Butterfly PeaCentrosema pubescens Benth. Jinjiang (2019, CATAS)Tropical zonesPerennialHerbaceous vine
      12Clitoria ternatea Linn. Sp. Pl.Asian pigeonwings, blue clitoria, butterfly peaAngustifolia Hochstetter ex Baker, major Paxton, Pleniflora Fantz, TernateaTropical zonesPerennialHerbaceous vine
      13Crotalaria albida Heyne ex Roth.Taiwan crotalariaalbida, Gengmanensis (Z. Wei & C.Y. Yang), Kangrensis A.A. AnsariSouthern AsiaPerennialHerbaceous
      14Crotalaria bractaeata Roxb. ex DC.Southern Asia, AmericaPerennialHerb or shrub
      15Crotalaria ferruginea (Grah.) Benth.Rust-color crotalariaSouthern Asia, AmericaPerennialHerb
      16Crotalaria retusa Linn.Large yellow rattlebox, rattleweedIndica Nampy & Sibichen, retusa, Tunguensis (Lima) PolhillTropical zonesPerennialShrub
      17Dendrolobium triangulare(Retz.) Schindl.Southern AsiaPerennialShrub
      18Desmanthus virgatus (L.) Willd.Wild tantan, Hedge lucerneGlandulosus (L.) Willd.,1806; Depressus (Humb. & Bonpl. ex Willd.) B.L. Turner; VirgatusTropical zonesPerennialHerb or shrub
      19Erythrina corallodendron L.Cutlass BushBicolor Krukoff, Connata Krukoff, Corallodendron L,1753Sporadic spread in tropical zonesPerennialTree
      20Galactia elliptifoliola Merr.Hainan, ChinaPerennialHerbaceous vine
      21Indigofera chuniana Metc.Hainan, ChinaPerennialHerb or shrub
      22Indigofera enneaphylla Linn. Mant.Hainan, China, Indonesia, Papua New Guinea, AustraliaAnnual or perennialHerb
      23Indigofera galegoides DC.Southern AsiaPerennialShrub
      24Indigofera hirsuta Linn.Hairy IndigoTropical zonesAnnual or perennialHerb
      25Indigofera litoralis Chun & T.C.ChenTropical zones of ChinaPerennialHerb
      26Indigofera suffruticosa Mill.Anil IndigoCanescens (J.A. Schmidt) Lobin, SuffruticosaTropical zonesPerennialShrub
      27Leucaena leucocephala (Lam.) de Wit.Leucaena, Lead Tree, CassieReyan No. 1Tropical zonesPerennialShrub or tree
      28Macroptilium atropurpureum (L.) Urb.Purple BeanSiratroTropical zonesAnnual or perennialHerb
      29Melilotus indicus (L.) All.Annual Melilot, Indian sweet-clover,Indicus, prostratus P.C. Palau, Tommasini (Jord.) O.E. SchulzWorld wideAnnualHerb
      30Melilotus officinalis (L.) Pall.Yellow sweet-clover, common yellow melilotWorld widePerennialHerb
      31Melilotus siculus (Turra) B.D.Jacks.Messina, NeptuneEurope and
      northern Australia
      Annual or perennialHerb
      32Pongamia pinnata (L.) PierreIndian Beech, Pongam treeHannii Domin, minor (Benth.) Domin, pinnata, Typica DominSouthern Asia and northern AustraliaPerennialTree
      33Pycnospora lutescens (Poir) Schindl.Southern Asia and northern AustraliaPerennialHerb or shrub
      34Senna bicapsularis (L.) Roxb.ChristmasbushAugusti (Harms) H.S. Irwin & Barneby, BicapsularisTropical zones of south America and southern AfricaPerennialShrub
      35Sesbania cannabina (Retz.) Pers.Yellow Pea Bush, DhainchaSericeaSouthern Asia and northern AustraliaAnnual or perennialHerb or shrub
      36Sesbania rostrata Bremek. & ObermAfricaAnnual or perennialHerb
      37Sesbania sesban (L.) Merr.Common SesbanConcolor (Wight & Arn.) Baquar; Bicolor (Wight & Arn.) FW. Andrews; Nubica Chiov; sesban (L.) Merr,1912; Zambesiaca J.B. GillettAfrica, India,
      southern America
      and China
      PerennialShrub
      38Stylosanthes guianensis (Aubl.) Sw.StyloReyan No. 20, 21, 22, 24, 25Tropical zones of Africa, Asia-pacific region and south AmericaPerennialShrub
      39Swainsona formosaSturt's Desert PeaAustraliaPerennialHerb
      40Tephrosia purpurea (Linn.) Pers. Syn. Pl.Sarphonk, wild indigoAngustissima B.L. Rob., Brevidens Benth., Elongata Craib, Gracilis Tackholm & Boulos, Leptostachya (DC.) Brummitt, Pubescens Baker, Queenslandica Domin, sericea Benth., Yunnanensis Z. WeiTropical zonesPerennialHerb
      41Teramnus labialis (Linn.f.) Spreng.Blue wissAbyssinicus (Hochst. ex A. Rich.) Verdc., Acutus Verdc., Arabicus Verdc., Labialis, Somalensis VatkeTropical zonesPerennialHerb
      42Trifolium fragiferum L.Strawberry cloverSalinaSubtropical zones
      of north America, Europe, east Asia, southern Australia and New Zealand
      PerennialHerb
      43Uraria lagopodiodies (Linn.) Desv.ex DC.Southern Asia and northern AustraliaPerennialShrub
      44Vigna marina (Burm.) Merr.Beachpeatropical zonesPerennialHerbaceous vine
      * Obtained from www.gbif.org/species

      There is quite a rich diversity of salinity tolerant species in coastlines of tropical regions, with six different species identified as high salinity tolerant (Table 2, No. 9, 29, 32, 34, 35, 44), 17 as moderate salinity tolerant (Table 2, No. 1−7, 11−12, 16, 30−31, 36−39, 42) and 21 species predicted as salinity tolerant but need to be further proven (Table 2, No. 8, 10, 13−15, 17−28, 33, 40−41, 43).

      Table 2.  Tolerances of current salinity tolerant forage legume species.

      No.Scientific nameSalinity tolerantDrought tolerantAcid
      tolerant
      Shade
      tolerant
      Waterlogging
      tolerant
      Frost
      tolerant
      Reference
      1Abrus precatorius L.XXX[55]
      2Acacia dealbata LinkXXX[7]
      3Acacia nilotica (L.) Willd. ex DelileXXX[25]
      4Alysicarpus vaginalis (L.) DC.XXXhttps://extension.msstate.edu/content/alyceclover-alysicarpus-vaginalis
      5Arachis pintoi Krapov. & W.C.Greg.XXXXwww.tropseeds.com/arachis-pintoi
      6Cajanus cajan (L.) Millsp.XXX[56]
      7Calopogonium mucunoides Desv.XX[57]
      8Canavalia ensifomis (L.) DCpotential*XXXpfaf.org/user/Plant.aspx?LatinName=Centrosema+pubescens
      9Canavalia rosea (Sw.) DC.X XXX[58]
      10Cassia pumila Lam.Potential*XX[59]
      11Centrosema pubescens Benth.XXX[60]
      12Clitoria ternatea Linn. Sp. Pl.XXXX[61]
      13Crotalaria albida Heyne ex Roth.Potential*XXhttps://baike.baidu.com/item/%E5%93%8D%E9%93%83%E8%B1%86/4860050?fromModule=lemma-qiyi_sense-lemma
      14Crotalaria bractaeata Roxb. ex DC.Potential*
      15Crotalaria ferruginea (Grah.) Benth.Potential*
      16Crotalaria retusa Linn.XX[62,63]
      17Dendrolobium triangulare(Retz.) Schindl.Potential*XX[64]
      18Desmanthus virgatus (L.) Willd.Potential*
      19Erythrina corallodendron L.Potential*XXXhttps://baike.baidu.com/item/%E9%BE%99%E7%89%99%E8%8A%B1/3567229?fr=kg_general
      20Galactia elliptifoliola Merr.Potential*
      21Indigofera chuniana Metc.Potential*Xhttps://baike.baidu.com/item/%E7%96%8F%E8%8A%B1%E6%9C%A8%E8%93%9D/1483435?fr=kg_general
      22Indigofera enneaphylla Linn. Mant.Potential*Xhttps://baike.baidu.com/item/%E4%B9%9D%E5%8F%B6%E6%9C%A8%E8%93%9D/7264010?fr=aladdin
      23Indigofera galegoides DC.Potential*
      24Indigofera hirsuta Linn.Potential*XXhttps://baike.baidu.com/item/%E7%A1%AC%E6%AF%9B%E6%9C%A8%E8%93%9D?fromModule=lemma_search-box
      25Indigofera litoralis Chun & T.C.ChenPotential*XXhttps://baike.baidu.com/item/%E6%BB%A8%E6%B5%B7%E6%9C%A8%E8%93%9D/7181556?fr=aladdin
      26Indigofera suffruticosa Mill.Potential*X[65]
      27Leucaena leucocephala (Lam.) de Wit.Potential*X[25] www.nparks.gov.sg/florafaunaweb/flora/3/4/3471
      28Macroptilium atropurpureum (L.) Urb.Potential*XXX[60]
      29Melilotus indicus (L.) All.X XXX[66,67]
      30Melilotus officinalis (L.) Pall.XXX[7,68]
      31Melilotus siculus (Turra) B.D.Jacks.XXX[7,53,69]
      32Pongamia pinnata (L.) PierreX XXXX[70]
      33Pycnospora lutescens (Poir) Schindl.Potential*
      34Senna bicapsularis (L.) Roxb.X XX XData to be published
      35Sesbania cannabina (Retz.) Pers.X XX XX[14,71,72]
      36Sesbania rostrata Bremek. & ObermXXX[7]
      37Sesbania sesban (L.) Merr.XX[7,25]
      38Stylosanthes guianensis (Aubl.) Sw.XXX[73,74]
      39Swainsona formosaXXX[75]
      40Tephrosia purpurea (Linn.) Pers. Syn. Pl.Potential*Xhttps://apps.worldagroforestry.org/treedb/AFTPDFS/Tephrosia_purpurea.PDF
      41Teramnus labialis (Linn.f.) Spreng.Potential*
      42Trifolium fragiferum L.XXX[67]
      43Uraria lagopodiodies (Linn.) Desv. ex DC.Potential*
      44Vigna marina (Burm.) Merr.X XX XX[13,76]
      Potential*: some germplasms collected from coastal areas with potential salinity tolerance and kept in the seed bank of Prataculturae Research Centre, Tropical Crops Genetic Resources Institute, Chinese Academy of Tropical Agricultural Sciences (CATAS). X means stress tolerant; XX means high stress tolerant.

      One important additional factor to consider is that some saline soils are marshes, which means that forage legumes integrated in such areas will also need to show waterlogging tolerance. Similar to what was observed for salinity tolerance, many reports have been published to explore legume waterlogging tolerance and legume-rhizobia symbiotic models for waterlogging tolerance[4852], legume species Canavalia ensifomis, Centrosema pubescens, Indigofera hirsute, Indigofera litoralis, Macroptilium atropurpureum, Melilotus indicus, Melilotus siculus, Pongamia pinnata, Sesbania cannabina, Sesbania rostrata and Trifolium fragiferum may have the combined tolerance of waterlogging and salinity based on the summarized information (Table 2), previous reports also indicated that Melilotus siculus is a very promising fodder for saline and waterlogged soils[53,54]. Researchers should pay more attention to legumes combining the traits of salinity and waterlogging tolerance and their field testing.

      Some of the listed legume species are tolerant to other abiotic stresses including drought tolerance, acidity tolerance, shade tolerance and frost tolerance (Table 2), drought tolerance is also a very import characteristic compared to salinity and waterlogging.

      There is high productivity diversity among the 44 legume species, eight species Alysicarpus vaginalis (4−6 t DW/ha/y), Cajanus cajan (3.175−6.515 t DW/ha/y), Calopogonium mucunoides (4−5 t DW/ha/y), Dendrolobium triangulare (4−5 t DW/ha/y), Indigofera hirsuta (3−6 t DW/ha/y), Macroptilium atropurpureum (2.4−5.5 t DW/ha/y), Stylosanthes guianensis (4−5 t DW/ha/y) and Trifolium fragiferum (4.31−5.19 t DW/ha/y) had relative high productivity compared to other species. The nutritional value of these legumes also varies among species, for instance, the maximum crude protein content of Sesbania sesban, Trifolium fragiferum, Macroptilium atropurpureum and Teramnus labialis are more than 20%. Further evaluation, including other nutrition values, chemical composition and feeding experiments should be conducted to test acceptability to animals and performance of livestock.

      Few studies exist regarding the nitrogen fixation efficiency of salinity tolerant legumes even though it is an important indicator for their utilization. Among the 44 species, only 11 species have been reported to have nitrogen fixation efficiency, Sesbania cannabina (949−1,040.25 kg N/ha/y), Arachis pintoi (300 kg/ha/y), Centrosema pubescens (120−270 kg N/ha/y) and Tephrosia purpurea (202.23 kg N/ha/y) had higher nitrogen fixation efficiency[7779] (www.tropseeds.com/arachis-pintoi/). We also found very few studies on salinity tolerant rhizobia associated with the listed legumes, most reported rhizobia could tolerate to a salinity concentration higher than 300 mM NaCl (Table 3).

      Table 3.  Productivity, nutrition value, BNF and salinity tolerance rhizobia of current tolerant forage legume species.

      No.Scientific nameProductivityLeaf crude proteinNitrogen fixation efficiencySalt tolerant rhizobiaReference
      1Abrus precatorius L.16.28%[80]
      2Acacia dealbata Link1.2−4.0 t DW/ha/y40 kg N/ha/y[81, 82]
      3Acacia nilotica (L.) Willd. ex Delile3.22 t DW/ha/y13.92%[8385]
      4Alysicarpus vaginalis (L.) DC.4–6 t DW/ha/y17.91%https://apps.lucidcentral.org/tropical_forages, https://extension.msstate.edu/content/alyceclover-alysicarpus-vaginalis
      5Arachis pintoi Krapov. & W.C.Greg.3−4 t DW t/ha/y17%-20%300 kg/ha/ywww.tropseeds.com/arachis-pintoi/
      6Cajanus cajan (L.) Millsp.3.175−6.515 t DM/ha/y[86]
      7Calopogonium mucunoides Desv.4−5 t DW/ha/ylow[57,87]
      8Canavalia ensifomis (L.) DC
      9Canavalia rosea (Sw.) DC.1.0−4.6 t DW/ha/y15%−20%Some strains tolerant to 500−600 mM NaCl[88,89]
      10Cassia pumila Lam.
      11Centrosema pubescens Benth.1.6−2.8 t DW /ha/y21.36%−23.34%120−270 kg N/ha/y[78]
      12Clitoria ternatea Linn. Sp. Pl.1.2−3.6 t DW /ha/y14%−20%Jd19 Rhizobium strain[90,91]
      13Crotalaria albida Heyne ex Roth.
      14Crotalaria bractaeata Roxb. ex DC.
      15Crotalaria ferruginea (Grah.) Benth.
      16Crotalaria retusa Linn.14.6%−18.0%[63]
      17Dendrolobium triangulare(Retz.) Schindl.4−5 t DW/ha/yAverage 13.43%[92]
      18Desmanthus virgatus (L.) Willd.3.98 t DW/ha/yAverage 15.20%[93]
      19Erythrina corallodendron L.
      20Galactia elliptifoliola Merr.2.0−3.5 t DW/ha/y[94]
      21Indigofera chuniana Metc.2−4 t DW/ha/yDate to be published
      22Indigofera enneaphylla Linn. Mant.3−4 t DW/ha/y10.7%[95]
      23Indigofera galegoides DC.Average 3.26% for total N[96]
      24Indigofera hirsuta Linn.3−6 t DW/ha/y1.7−1.9% for total N[96]
      25Indigofera litoralis Chun & T.C.Chen
      26Indigofera suffruticosa Mill.2−4 t DW/ha/yAverage 3.77 for total N[96]
      27Leucaena leucocephala (Lam.) de Wit.3.4 t DW/ha/y22.8%−25.9%76 kg N/ha/y[97, 98]
      28Macroptilium atropurpureum (L.) Urb.2.4–5.5 t DW/ha/y13.73%−28.2%62−178 kg N/ha/y[99101]
      29Melilotus indicus (L.) All.3.8 t DW/ha/ySome strain tolerant to 6% NaCl[66, 102]
      30Melilotus officinalis (L.) Pall.14.5%−19.4%Add 80–130 pounds/acre of nitrogen to soil[103, 104]
      www.sciencedirect.com/topics/agricultural-and-biological-sciences/melilotus-officinalis
      31Melilotus siculus (Turra) B.D.Jacks.
      32Pongamia pinnata (L.) Pierre
      33Pycnospora lutescens (Poir) Schindl.
      34Senna bicapsularis (L.) Roxb.
      35Sesbania cannabina (Retz.) Pers.2.46−3.55 t DW/ha/y949−1,040.25 kg N/ha/ySome strains tolerant to 5.0% (w/v) NaCl[77, 105, 106] www.healthbenefitstimes.com/sesbania
      36Sesbania rostrata Bremek. & Oberm1.06−2.19 t DW/ha/yAverage 19.9%90−219 kg N/ha/y[77,107]
      37Sesbania sesban (L.) Merr.2.39−2.59 kg DW/ha/y20%−25%42.6−109.5 kg N/ha/y[108,109]
      38Stylosanthes guianensis (Aubl.) Sw.4−5 t DW /ha/y14%−20%96−122 kg N/ha/yBradyrhizobium strain RJS9-2 tolerant to 350 mM NaCl[46,110]
      39Swainsona formosa
      40Tephrosia purpurea (Linn.) Pers. Syn. Pl.16.27%202.23 kg N/ha/ySome strains tolerant to 2.5%−3% of NaCl[79,111]
      41Teramnus labialis (Linn.f.) Spreng.3−4 t DM/ha/y22.86%[112,113]
      42Trifolium fragiferum L.4.31−5.19 t DM/ha/y14.9%−25.7%[114,115]
      43Uraria lagopodiodies (Linn.) Desv.ex DC.
      44Vigna marina (Burm.) Merr.2.0−4.0 t DW/ha/y13%−20%Some strains tolerant to 600 mM NaCl[13,116]

      From the 44 summarized legumes, 95.5% have potential to be utilized as forage, Abrus precatorius and Crotalaria retusa contain toxic substances such as monocrotaline which is not safe to use as forage. Eighty four point one percent have potential as green manure, the species Abrus precatorius, Acacia dealbata, Acacia nilotica, Leucaena leucocephala and Pongamia pinnata are too big to be green manure. Eleven point four percent of the species may be developed for food, 59.1% as medicine and 40.9% for ornamental purposes (Table 4).

      Table 4.  Utilization of current salinity tolerant forage legume species.

      No.Scientific nameForageGreen manureFoodMedicineOrnamentalReference
      1Abrus precatorius L.XX[118]
      2Acacia dealbata LinkXXX[119]
      3Acacia nilotica (L.) Willd. ex DelileXX[84]
      4Alysicarpus vaginalis (L.) DC.XXXhttps://apps.lucidcentral.org/tropical_forages
      5Arachis pintoi Krapov. & W.C.Greg.XXXhttps://apps.lucidcentral.org/tropical_forages, www.tropseeds.com/
      6Cajanus cajan (L.) Millsp.XXXX[120]
      7Calopogonium mucunoides Desv.XX[121]
      8Canavalia ensifomis (L.) DCXXXX[122]
      9Canavalia rosea (Sw.) DC.XXXXX[89]
      10Cassia pumila Lam.XXX[59]
      11Centrosema pubescens Benth.XX[78]
      12Clitoria ternatea Linn. Sp. Pl.XXXX[90,123]
      13Crotalaria albida Heyne ex Roth.XX[124]
      14Crotalaria bractaeata Roxb. ex DC.XXXhttps://plants.ces.ncsu.edu/plants/crotalaria-spectabilis/
      15Crotalaria ferruginea (Grah.) Benth.XXX[125]
      16Crotalaria retusa Linn.XXXhttps://baike.baidu.com/item/%E5%90%8A%E8%A3%99%E8%8D%89?fromModule=lemma_search-box#reference-[1]-3529418-wrap
      17Dendrolobium triangulare(Retz.) Schindl.XXXXhttps://baike.baidu.com/item/%E5%81%87%E6%9C%A8%E8%B1%86/23437879?fromModule=lemma-qiyi_sense-lemma
      18Desmanthus virgatus (L.) Willd.XX[93]
      19Erythrina corallodendron L.XXXhttps://baike.baidu.com/item/%E9%BE%99%E7%89%99%E8%8A%B1/3567229?fr=kg_general
      20Galactia elliptifoliola Merr.XX[94]
      21Indigofera chuniana Metc.XXXhttps://baike.baidu.com/item/%E7%96%8F%E8%8A%B1%E6%9C%A8%E8%93%9D/1483435?fr=kg_general
      22Indigofera enneaphylla Linn. Mant.XXXX[126]
      23Indigofera galegoides DC.XXXX[96]
      24Indigofera hirsuta Linn.XXX[96]
      25Indigofera litoralis Chun & T.C.ChenXXXXhttps://baike.baidu.com/item/%E6%BB%A8%E6%B5%B7%E6%9C%A8%E8%93%9D/7181556?fr=aladdin
      26Indigofera suffruticosa Mill.XXX[96]
      27Leucaena leucocephala (Lam.) de Wit.XXX[97]
      28Macroptilium atropurpureum (L.) Urb.XX[99]
      29Melilotus indicus (L.) All.XXX[66]
      30Melilotus officinalis (L.) Pall.XXXX[103]
      31Melilotus siculus (Turra) B.D.Jacks.XXX[10]
      32Pongamia pinnata (L.) PierreXX[70]
      33Pycnospora lutescens (Poir) Schindl.XX[127]
      34Senna bicapsularis (L.) Roxb.XXX[128]
      35Sesbania cannabina (Retz.) Pers.XXX[14]
      36Sesbania rostrata Bremek. & ObermXX[107]
      37Sesbania sesban (L.) Merr.XX[109]
      38Stylosanthes guianensis (Aubl.) Sw.[110]
      39Swainsona formosaXXX[75]
      40Tephrosia purpurea (Linn.) Pers. Syn. Pl.XXXhttps://apps.worldagroforestry.org/treedb/AFTPDFS/Tephrosia_purpurea.PDF
      41Teramnus labialis (Linn.f.) Spreng.XXX[112]
      42Trifolium fragiferum L.XX[115]
      43Uraria lagopodiodies (Linn.) Desv.ex DC.XXhttps://powo.science.kew.org/taxon/524403-1
      44Vigna marina (Burm.) Merr.XXXXX[129]
      X means can be used.

      When served as forage, these legumes can either be used in a cut and carry system or grazing, depending on the size of the plots, other crops grown in the same area or farmers' preference. However, in the case of forage, the nutrients contained in the plants do not benefit the soil: there is a trade-off between soil rehabilitation and livelihood benefits[117]. A compromise is to alternate use for forage or green manure at different times if space allows. A good strategy would be to return animal manure to the soil, eventually following a composting phase. When used as green manure, these legumes can be intercropped with fruit trees or grown in rotation with salinity tolerant food crops (cereals or tubers). They can then protect the soil (moisture conservation, reduce erosion etc.), decompose and increase soil organic matter and nitrogen content.

      Adoption of salinity tolerant legumes in coastal areas is limited. Very few studies have reported the adoption of these crops. In Western Australia, salinity tolerant pasture legumes and grasses have been promoted to improve the productivity and profitability of saline land and salt bush-based pastures (www.agric.wa.gov.au/soil-salinity/pasture-legumes-and-grasses-saline-land-western-australia). In south-eastern Tunisia, a study on farmers' willingness to adopt salinity-tolerant forage crops showed that off-farm income availability and flock size significantly affected farmers' willingness to adopt salinity-tolerant forages[130]. Testing of halophytes and salinity-tolerant plants as potential forage for ruminants was carried in the Near East region, Egypt, but few of them are legumes[131]. However, adoption barriers typical for cover crops can be expected such as measures related to soil management, impact on yields and income are not immediate, making it difficult for farmers to invest in the technology[132]. When used as forage, the likelihood of adoption is higher as increases in milk production and weight gain can be quickly observed. One main barrier is the availability of planting material, it's a challenge for the farmers to find planting legumes with high salinity tolerant, high biomass and high nutritive value.

    • Salinity tolerant legumes have a great potential to reclaim sea-level-rise affected tropical coastal agroecosystems, support bridging the protein gap in an environmentally-friendly manner and increase smallholder farmers' income (Fig. 1). Although usages and some benefits have been documented, detailed information is lacking for many of them. Tolerance combinations for locations with multiple abiotic stresses like marshes also need to be further explored. Among the species reviewed, Sesbania cannabina (Retz.) Pers., Melilotus indicus (L.) All. and Vigna marina (Burm.) Merr. are good candidates but there are still gaps in the research before it can be promoted at scale. Gaps include the nitrogen fixation efficiency and soil reclamation potential, as well as the impact on farming systems and livelihoods in a holistic way. The selection of salinity-tolerant rhizobia symbiosis, which are more effective than when both legumes and rhizobia are selected separately, is particularly crucial.

      Figure 1. 

      Inter-cropping system with salinity tolerant legumes on coastal ecosystems.

      The integration of salinity tolerant legumes into coastal farming systems will be subject to country-specific adoption barriers and system requirements. To ensure livelihood benefits for millions of smallholder farmers in tropical coastal agroecosystems, commitment and support from government and public services are necessary to address both seed system and extension needs, through the provision of adequate incentives, policies and development efforts.

      • This work was funded by the National Science and Technology Basic Resources Investigation Project (2017FY100600), Feeds and Forages flagship of the CGIAR Research Program on Livestock, the Key Research and Development Program of Hainan (321RC646), China Agriculture Research System of MOF and MARA (CARS-22). We warmly thank Ms. Andrea Ramírez and Mr. José Luis Urrea Benitez for the design of Fig. 1.

      • The authors declare that they have no conflict of interest.

      • # These authors contributed equally: Yiming Liu, Mary Atieno

      • Copyright: © 2022 by the author(s). Published by Maximum Academic Press, Fayetteville, GA. This article is an open access article distributed under Creative Commons Attribution License (CC BY 4.0), visit https://creativecommons.org/licenses/by/4.0/.
    Figure (1)  Table (4) References (132)
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    Liu Y, Atieno M, Cardoso JA, Yang H, Xu Bin, et al. 2022. Mining and utilization of salinity tolerant legumes in tropical coastal agroecosystems: An overview. Grass Research 2:10 doi: 10.48130/GR-2022-0010
    Liu Y, Atieno M, Cardoso JA, Yang H, Xu Bin, et al. 2022. Mining and utilization of salinity tolerant legumes in tropical coastal agroecosystems: An overview. Grass Research 2:10 doi: 10.48130/GR-2022-0010

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