Abstract
Actinorhizal symbiosis naturally harbours beneficial categories of diverse plant growth promoting microorganisms (PGPMs), including the Frankia species. The beneficial microorganisms can be used as efficient, non-chemical and sustainable alternatives for adopting effective soil restoration programmes and revegetation schedules in chemical and industrial-contaminated sites, including treating degraded lands contaminated with toxic chemicals and pesticides. It has been proposed that the interactions between the microbial gene pool are of immense agricultural significance that would facilitate an improvement in the health, hygiene and nutrient acquisition pathway of native soil. The present review is focused on exploiting the hitherto-unexplored Frankia-actinorhizal symbiosis with due interest for their application in soil restoration programmes, including the reclamation of degraded lands. This opens up new insights for the development of sustainability in forestry and plantation research. Additionally, it would promise an improvement in plant growth and vigour, hygiene, and other parameters related to crop yield, such as plant biomass, root/shoot ratio, crop yield, and so on. Novel and putative microorganisms isolated from the actinorhizal may be used for bio-transformation of allelochemicals and toxic heavy metals into compounds with modified biological properties, opening up novel avenues for mediating microbial degradation of putative allelochemicals that would otherwise accumulate at phytotoxic levels in soil. Endophyte-host specificities, the phylogeny of Frankia, and the conservation of unique endemic plant genetic resources like actinorhizal plants, are of paramount significance in the advancement of genomics, metabolomics and phenomics.
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All data is provided in tables and figures.
Abbreviations
- ATP:
-
Adenosine triphosphate
- AMF:
-
Arbuscular mycorrhizal fungi
- BNF:
-
Biological nitrogen fixation
- CgAUX1 :
-
Auxin influx carrier
- CgRHDF:
-
The root hair deforming factor
- CgNINA:
-
NIN activating factor
- CBD:
-
The Convention on Biological Diversity
- CDMs:
-
Cellulose degrading microorganisms
- ePGPR:
-
Extracellular plant growth promoting rhizobacteria
- ECM:
-
Ectomycorrhizal
- ETC:
-
Electron transport chain
- hbs :
-
Haemoglobin
- IAA:
-
Indole-3-acetic acid
- ISR:
-
Induction of systematic resistance
- iPGPR:
-
Intracellular plant growth promoting rhizobacteria
- GS-GOGAT:
-
The glutamine synthetase-glutamate synthase cycle
- KMMs:
-
Potash mobilising microorganisms
- NFs:
-
Nod factors
- NFMs:
-
Nitrogen fixing microorganisms
- PGP traits:
-
Plant growth promoting traits
- PGPMs:
-
Plant growth promoting microorganisms
- PAH:
-
Polyaromatic hydrocarbon
- PSMs:
-
Phosphate solubilising microorganisms
- ROS:
-
Reactive oxygen species
- ZSMs:
-
Zinc solubilising microorganisms
References
Abdel-Lateif K, Vaissayre V, Gherbi H, Verries C, Meudec E, Perrine-Walker F, Cheynier V, Svistoonoff S, Franche C, Bogusz D et al (2013) Silencing of the chalcone synthase gene in Casuarina highlights the important role of flavonoids during nodulation. New Phytol 199:1012–1021
Afkhami ME, Almeida BK, Hernandez DJ, Kiesewetter KN, Revillini DP (2020) Tripartite mutualisms as models for understanding plant–microbial interactions. Curr Opin Plant Biol 56:28–36. https://doi.org/10.1016/j.pbi.2020.02.003
Ahmadiani A, Hosseiny J, Semnanian S, Javan M, Saeedi F, Kamalinejad M, Saremi S (2000) Antinociceptive and anti-inflammatory effects of Elaeagnus angustifolia fruit extract. J Ethnopharmacol 72:287–292. https://doi.org/10.1016/S0378-8741(00)00222-1
Andrade DS, Leal AC, Ramos ALM et al (2015) Growth of Casuarina cunninghamiana inoculated with arbuscular mycorrhizal fungi and Frankia actinomycetes. Symbiosis 66:65–73. https://doi.org/10.1007/s13199-015-0335-1
Auguy F, Abdel-Lateif K, Doumas P, Badin P, Guerin V, Bogusz D, Hocher V (2011) Activation of the isoflavonoid pathway in actinorhizal symbioses. Funct Plant Biol 38(9):690–696. https://doi.org/10.1071/FP11014
Battenberg K, Hayashi M (2022) Evolution of root nodule symbiosis: Focusing on the transcriptional regulation from the genomic point of view. Plant Biotechnol 39(1):79–83. https://doi.org/10.5511/plantbiotechnology.22.0127a
Battenberg K, Wren JA, Hillman J, Edwards J, Liujing Huang L, Berry AM (2016) The Influence of the Host Plant Is the Major Ecological Determinant of the Presence of Nitrogen-Fixing Root Nodule Symbiont Cluster II Frankia Species in Soil. Appl Environ Microbiol 83(1):e02661-e2716. https://doi.org/10.1128/AEM.02661-16
Becerra AG, Menoyo E, Lett I, Li CY (2009) Alnus acuminata in dual symbiosis with Frankia and two different ectomycorrhizal fungi (Alpova austroalnicola and Alpova diplophloeus) growing in soilless growth medium. Symbiosis 47:85–92. https://doi.org/10.1007/BF03182291
Begum N, Qin C, Ahanger MA, Raza S, Khan MI, Ashraf M, Ahmed N, Zhang L (2019) Role of Arbuscular Mycorrhizal Fungi in Plant Growth Regulation: Implications in Abiotic Stress Tolerance. Front Plant Sci 10:1068. https://doi.org/10.3389/fpls.2019.01068
Berckx F, Nguyen TV, Bandong CM et al (2022) A tale of two lineages: how the strains of the earliest divergent symbiotic Frankia clade spread over the world. BMC Genomics 23:602. https://doi.org/10.1186/s12864-022-08838-5
Berry AM, Harriott OT, Moreau RA, Osman SF, Benson DR, Jones AD (1993) Hopanoid lipids compose the Frankia vesicle envelope, presumptive barrier of oxygen diffusion to nitrogenase. Proc Natl Acad Sci USA 13:6091–6094. https://doi.org/10.1073/pnas.90.13.6091
Bhattacharyya PN, Jha DK (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J Microbiol Biotechnol 28:1327–1350. https://doi.org/10.1007/s11274-011-0979-9
Bhattacharyya PN, Tanti B, Barman P, Jha DK (2014) Culture-independent metagenomic approach to characterize the surface and subsurface soil bacterial community in the Brahmaputra valley, Assam, North-East India, an Indo-Burma mega-biodiversity hotspot. World J Microbiol Biotechnol 30(2):519–528. https://doi.org/10.1007/s11274-013-1467-1
Bhattacharyya PN, Goswami MP, Bhattacharyya LH (2016) Perspective of beneficial microbes in agriculture under changing climatic scenario: A review. J Phytol 8:26–41. https://doi.org/10.19071/jp.2016.v8.3022
Bhattacharyya LH, Bhattacharyya PN (2021) Actinorhizal plants, Elaeagnus latifolia L. conservation: Perspectives in reclamation of degraded land including tea soil. LAP LAMBERT Academic Publishing, Omniscriptum Publishing Group, Chisinau 2068, Republic of Moldova Europe, pp 1–125
Bhattacharyya, PN, Sarmah SR (2018) The role of tea soil microflora in tea cultivation. In: Sharma VS, Kumudini Gunasekare MT (eds) Global Tea Science, Burleigh Dodds Science Publishing, Sawston, Cambridge, UK, 135–167. https://doi.org/10.19103/AS.2017.0036.24
Bhattacharyya PN (2012) Diversity of microorganisms in the surface and subsurface soil of the Jia Bharali River catchment area of Brahmaputra plains. PhD Thesis, Gauhati University, Guwahati, Assam, India, p 6
Bogusz D, Claudine Franche (2020) Frankia and the actinorhizal symbiosis. In: Sharma V, Salwan R, Al-Ani LKT (eds) Molecular Aspects of Plant Beneficial Microbes in Agriculture, Academic Press, pp. 367–380. https://doi.org/10.1016/B978-0-12-818469-1.00030-4
Bonzini M, Leso V, Iavicoli I (2022) Towards a toxic-free environment: perspectives for chemical risk assessment approaches. Med Lav 113(1):e2022004. https://doi.org/10.23749/mdl.v113i1
BouizgarneB, Oufdou K, Ouhdouch Y (2015) Actinorhizal and Rhizobial-Legume Symbioses for Alleviation of Abiotic Stresses. In: Arora N. (eds) Plant Microbes Symbiosis: Applied Facets. Springer, New Delhi. https://doi.org/10.1007/978-81-322-2068-8_14
Bungau S, Behl T, Aleya L et al (2021) Expatiating the impact of anthropogenic aspects and climatic factors on long-term soil monitoring and management. Environ Sci Pollut Res 28:30528–30550. https://doi.org/10.1007/s11356-021-14127-7
Carrasco A, Schwencke J, Caru M (1992) Isolation of Frankia from nodules of Trevoa trinervis: Ultrastructural characterization. Can J Microbiol 38:174–180
Chaia EE, Wall LG, Huss-Danell K (2010) Life in soil by the actinorhizal root nodule endophyte Frankia. A Review Symbiosis 51:201–226. https://doi.org/10.1007/s13199-010-0086-y
Champion A et al (2015) Inhibition of Auxin Signaling in Frankia Species-Infected Cells in Casuarina glauca Nodules Leads to Increased Nodulation. Plant Physiol 167(3):1149–1157. https://doi.org/10.1104/pp.114.255307
Chen H, Renault S, Markham J (2020) The effect of Frankia and multiple ectomycorrhizal fungal species on Alnus growing in low fertility soil. Symbiosis 80:207–215. https://doi.org/10.1007/s13199-020-00666-z
Chen QL, Hu HW, He ZY et al (2021) Potential of indigenous crop microbiomes for sustainable agriculture. Nat Food 2:233–240. https://doi.org/10.1038/s43016-021-00253-5
Cissoko M, Hocher V, Gherbi H, Gully D et al (2018) Actinorhizal Signaling Molecules: Frankia Root Hair Deforming Factor Shares Properties with NIN Inducing Factor. Front Plant Sci 9:1494. https://doi.org/10.3389/fpls.2018.01494
Clawson ML, Caru M, Benson DR (1998) Diversity of Frankia strains in root nodules of plants from the families Elaeagnaceae and Rhamnaceae. Appl Environ Microbiol 64(9):3539–3543. https://doi.org/10.1128/AEM.64.9.3539-3543.1998
Coelho N, Gonçalves S, Romano A (2020) Endemic Plant Species Conservation: Biotechnological Approaches. Plants (Basel) 9(3):345. https://doi.org/10.3390/plants903034
Cusato MS, Tortosa RD, Valiente L, Barneix AJ, Puelles MM (2007) Effects of Zn2+ on nodulation and growth of a South American actinorhizal plant, Discaria americana (Rhamnaceae). World J Microbiol Biotechnol 23:771–777. https://doi.org/10.1007/s11274-006-9295-1
Dar GH, Khuroo AA (2020) An Introduction to Biodiversity of the Himalaya: Jammu and Kashmir State. In: Dar G, Khuroo A (eds) Biodiversity of the Himalaya: Jammu and Kashmir State. Topics Biodiversity Conservation, vol 18, Springer, Singapore. https://doi.org/10.1007/978-981-32-9174-4_1
Dar JA, Kareem M, Zargar SM, Wani AA, Rasool S, Bhat KA (2020) Strategies for conservation of genetic resources. In: Salgotra R, Zargar S. (eds) Rediscovery of Genetic and Genomic Resources for Future Food Security. Springer, Singapore. https://doi.org/10.1007/978-981-15-0156-2_12
Das AK, Tag H, Bharali P (2016) Bio-Resources of Northeast India: Sustainable Utilization and Challenges. In: Purkayastha J (eds) Bioprospecting of Indigenous Bioresources of North-East India. Springer, Singapore. https://doi.org/10.1007/978-981-10-0620-3_2
de Faria MR, Costa LSAS, Chiaramonte JB et al (2021) The rhizosphere microbiome: functions, dynamics, and role in plant protection. Trop Plant Pathol 46:13–25. https://doi.org/10.1007/s40858-020-00390-5
Deguine JP, Aubertot JN, Flor RJ et al (2021) Integrated pest management: good intentions, hard realities. A Review Agron Sustain Dev 41:38. https://doi.org/10.1007/s13593-021-00689-w
Deicke M, Mohr JF, Roy S, Herzsprung P, Bellenger JP, Wichard T (2019) Metallophore profiling of nitrogen-fixing Frankia spp. to understand metal management in the rhizosphere of actinorhizal plants. Metallomics 11(4):810–821. https://doi.org/10.1039/c8mt00344k
Diagne N, Arumugam K, Ngom M et al. (2013) Use of Frankia and actinorhizal plants for degraded lands reclamation. Biomed Research International 948258. https://doi.org/10.1155/2013/948258
Diagne N et al (2015) Remediation of Heavy Metal-Contaminated Soils and Enhancement of Their Fertility with Actinorhizal Plants. In: Sherameti I, Varma A (eds) Heavy Metal Contamination of Soils. Soil Biology vol 44, Springer, Cham. https://doi.org/10.1007/978-3-319-14526-6_19
Diedhiou I, Diouf D (2018) Transcription factors network in root endosymbiosis establishment and development. World J Microbiol Biotechnol 34:37. https://doi.org/10.1007/s11274-018-2418-7
Dikshit KR, Dikshit JK (2014) Natural Vegetation: Forests and Grasslands of North-East India. In: North-East India: Land, People and Economy. Advances in Asian Human-Environmental Research. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-7055-3_9
Ding W (2022) The promotion of legume nodulation in plant-soil-microbe systems under phosphorus-limited conditions. Plant Soil 476:251–262. https://doi.org/10.1007/s11104-022-05564-5
Djighaly PI, Ngom D, Diagne N, Fall D et al (2020) Effect of Casuarina Plantations Inoculated with Arbuscular Mycorrhizal Fungi and Frankia on the Diversity of Herbaceous Vegetation in Saline Environments in Senegal. Diversity 12(8):293. https://doi.org/10.3390/d12080293
Domínguez-Nunez JA, Marta Berrocal-Lobo (2021) Application of microorganisms in forest plant. In: Rakshit A, Meena VS, Parihar M, Singh HB, Singh AK (eds) Biofertilizers, Woodhead Publishing, pp. 265–287. https://doi.org/10.1016/B978-0-12-821667-5.00026-9
Douglas A (2016) How multi-partner endosymbioses function. Nat Rev Microbiol 14:731–743. https://doi.org/10.1038/nrmicro.2016.151
Dwibedi V, Rath SK, Joshi M et al (2022) Microbial endophytes: application towards sustainable agriculture and food security. Appl Microbiol Biotechnol 106:5359–5384. https://doi.org/10.1007/s00253-022-12078-8
Feng Y, Xu P, Li B et al (2017) Ethylene promotes root hair growth through coordinated EIN3/EIL1 and RHD6/RSL1 activity in Arabidopsis. Proc Nat Aca Sci USA 114:13834–13839. https://doi.org/10.1073/pnas.1711723115
Figueiredo Md VB, Bonifacio A, Rodrigues AC, de Araujo FF (2016) Plant Growth-Promoting Rhizobacteria: Key Mechanisms of Action. In: Choudhary D, Varma A (eds) Microbial-mediated Induced Systemic Resistance in Plants. Springer, Singapore. https://doi.org/10.1007/978-981-10-0388-2_3
Froussart E, Bonneau J, Franche C, Bogusz D (2016) Recent advances in actinorhizal symbiosis signaling. Plant Mol Biol 90(6):613–622. https://doi.org/10.1007/s11103-016-0450-2
Gardner IC, Barrueco CR (1999) Mycorrhizal and actinorhizal biotechnology-problems and prospects. In: Varma A, Hock B (eds) Mycorrhiza, 2nd edn. Springer, Berlin. https://doi.org/10.1007/978-3-662-08897-5_21
Ghodhbane-Gtari F, D’Angelo T, Gueddou A, Ghazouani S, Gtari M, Tisa LS (2021) Alone Yet Not Alone: Frankia Lives Under the Same Roof with Other Bacteria in Actinorhizal Nodules. Front Microbiol 12:749760. https://doi.org/10.3389/fmicb.2021.749760
Gifford I, Vance S, Nguyen G, Berry AM (2019) A Stable Genetic Transformation System and Implications of the Type IV Restriction System in the Nitrogen-Fixing Plant Endosymbiont Frankia alni ACN14a. Front Microbiol 10:2230. https://doi.org/10.3389/fmicb.2019.02230
Gifford I, Battenberg K, Vaniya A, Wilson A, Tian L, Fiehn O, Berry AM (2018) Distinctive Patterns of Flavonoid Biosynthesis in Roots and Nodules of Datisca glomerata and Medicago spp. Revealed by Metabolomic and Gene Expression Profiles. Front Plant Sci 9:1463. https://doi.org/10.3389/fpls.2018.01463
Gtari M, Brusetti L, Skander G, Mora D, Boudabous A, Daffonchio D et al (2004) Isolation of Elaeagnus-compatible Frankia from soils collected in Tunisia. FEMS Microbiol Lett 234:349–355. https://doi.org/10.1016/j.femsle.2004.04.001
Gtari M, Ghodhbane-Gtari F, Nouioui I, Ktari A, Hezbri K, Mimouni W et al (2015) Cultivating the uncultured: growing the recalcitrant cluster-2 Frankia strains. Sci Rep 5:13112. https://doi.org/10.1038/srep13112
Gtari M (2022) Taxogenomic status of phylogenetically distant Frankia clusters warrants their elevation to the rank of genus: A description of Protofrankia gen. nov., Parafrankia gen. nov., and Pseudofrankia gen. nov. as three novel genera within the family Frankiaceae. Front Microbiol 13:1041425. https://doi.org/10.3389/fmicb.2022.1041425
Gueddou A, Sarker I, Sen A, Ghodhbane-Gtari F, Benson DR, Armengaud J, Gtari M (2022) Effect of actinorhizal root exudates on the proteomes of Frankia soli NRRL B-16219, a strain colonizing the root tissues of its actinorhizal host via intercellular pathway. Res Microbiol 173(1–2):103900. https://doi.org/10.1016/j.resmic.2021.103900
Gunthardt-Goerg MS, McQuattie CJ, Scheidegger C, Rhiner C, Matyssek R (1997) Ozone induced cytochemical and ultrastructural changes in leaf mesophyll cell walls. Can J for Res 27:453–463. https://doi.org/10.1139/x96-187
Gupta SM, Kumar K, Joshi RK, Gupta S, Bala M (2020) Frankia: A Promising N-Fixing Plant Growth Promoting Rhizobacteria (PGPR) Improved Drought Tolerance in Crops at Higher Altitude. In: Goel R, Soni R, Suyal D (eds) Microbiological Advancements for Higher Altitude Agro-Ecosystems and Sustainability. Rhizosphere Biology. Springer, Singapore. https://doi.org/10.1007/978-981-15-1902-4_20
Handique L. (2015) Actinorhizal, Endomycorrhizal and Endophytic microbiota associated with Elaeagnus latifolia L. rhizosphere and their role in its conservation and bioactive secondary metabolites production. Ph. D. Thesis, Forest Research Institute (Deemed) University, Dehradun, Uttarakhand, India. pp. 54–55
Hawkins JP, Oresnik IJ (2022) The Rhizobium-Legume Symbiosis: Co-opting Successful Stress Management. Front Plant Sci 12:796045. https://doi.org/10.3389/fpls.2021.796045
Hay AE, Herrera-Belaroussi A, Rey M, Fournier P, Normand P, Boubakri H (2020) Feedback Regulation of N Fixation in Frankia-Alnus Symbiosis Through Amino Acids Profiling in Field and Greenhouse Nodules. Mol Plant Microbe Interact 33(3):499–508. https://doi.org/10.1094/MPMI-10-19-0289-R
Hobohm C, Tucker CM (2014) The Increasing Importance of Endemism: Responsibility, the Media and Education. In: Hobohm C (eds) Endemism in Vascular Plants. Plant and Vegetation, vol 9. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-6913-7_1
Hocher V, Ngom M, Carre-Mlouka A et al (2019) Signalling in actinorhizal root nodule symbioses. Antonie Van Leeuwenhoek 112:23–29. https://doi.org/10.1007/s10482-018-1182-x
Holt JH (1994) Bergey’s manual of determinative bacteriology (9thedn) Lippincott. Williams and Wilkins, Philadelphia, PA, p 1994
Hoosbeek MR, Lukac M, Velthorst E, Smith AR, Godbold DL (2011) Free atmospheric CO2 enrichment increased above ground biomass but did not affect symbiotic N2-fixation and soil carbon dynamics in a mixed deciduous stand in Wales. Biogeoscience 8:353–364. https://doi.org/10.5194/BG-8-353-2011
Howard MM, Bass E, Chauta A et al (2022) Integrating plant-to-plant communication and rhizosphere microbial dynamics: ecological and evolutionary implications and a call for experimental rigor. ISME J 16:5–9. https://doi.org/10.1038/s41396-021-01063-0
Hu B, Flemetakis E, Liu Z, Hansch R, Rennenberg H (2023) Significance of nitrogen-fixing actinorhizal symbioses for restoration of depleted, degraded, and contaminated soil. Trends Plant Sci. https://doi.org/10.1016/j.tplants.2023.03.005
Ivanov VV, Stabnikov (2016) Basic concepts on biopolymers and biotechnological admixtures for eco-efficient construction materials. In: Fernando Pacheco-Torgal, Volodymyr Ivanov, Niranjan Karak, Henk Jonkers (eds) Biopolymers and Biotech Admixtures for Eco-Efficient Construction Materials, Woodhead Publishing, pp. 13–35. https://doi.org/10.1016/B978-0-08-100214-8.00002-6
Jalli R, Aravind J, Pandey A (2015) Conservation and Management of Endemic and Threatened Plant Species in India: An Overview. In: Bahadur B, Venkat Rajam M, Sahijram L, Krishnamurthy K (eds) Plant Biology and Biotechnology. Springer, New Delhi. https://doi.org/10.1007/978-81-322-2283-5_24
Kaiser MS (2021) Land Degradation: Causes, Impacts, and Interlinks with the Sustainable Development Goals. In: Leal Filho W, Azul AM, Brandli L, Ozuyar PG, Wall T (eds) Responsible Consumption and Production. Encyclopedia of the UN Sustainable Development Goals. Springer, Cham. https://doi.org/10.1007/978-3-319-71062-4_48-1
Karaca M, Ince AG (2019) Conservation of Biodiversity and Genetic Resources for Sustainable Agriculture. In: Farooq M, Pisante M. (eds) Innovations in Sustainable Agriculture. Springer, Cham. https://doi.org/10.1007/978-3-030-23169-9_12
Khare E, Swati Tyagi, Kishor Sureshbhai Patil (2020) Language of plant-microbe-microbe interactions in rhizospheric ecosystems. In: Vivek Sharma, Richa Salwan, Laith Khalil Tawfeeq Al-Ani (eds) Molecular Aspects of Plant Beneficial Microbes in Agriculture, Academic Press, pp. 59–76. https://doi.org/10.1016/B978-0-12-818469-1.00005-5
Knowlton S, Dawson JO (1983) Effects of Pseudomonas cepacia and cultural factors on the nodulation of Alnus rubra roots by Frankia. Can J Bot 61:2877–2882. https://doi.org/10.1139/b83-320
Kou-Giesbrecht S, Menge D (2019) Nitrogen-fixing trees could exacerbate climate change under elevated nitrogen deposition. Nat Commun 10:1493. https://doi.org/10.1038/s41467-019-09424-2
Kour D et al. (2019) Rhizospheric Microbiomes: Biodiversity, Mechanisms of Plant Growth Promotion, and Biotechnological Applications for Sustainable Agriculture. In: Kumar A, Meena V (eds) Plant Growth Promoting Rhizobacteria for Agricultural Sustainability. Springer, Singapore. https://doi.org/10.1007/978-981-13-7553-8_2
Ktari A, Gueddou A, Nouioui I, Miotello G, Sarkar I, Ghodhbane-Gtari F, Sen A, Armengaud J, Gtari M (2017) Host Plant Compatibility Shapes the Proteogenome of Frankia coriariae. Front Microbiol 8:720. https://doi.org/10.3389/fmicb.2017.00720
Kucho KI, Tamari D, Matsuyama S, Nabekura T, Tisa LS (2017) Nitrogen Fixation Mutants of the Actinobacterium Frankia Casuarinae CcI3. Microbes Environ 32(4):344–351. https://doi.org/10.1264/jsme2.ME17099
Kumar A, Dubey A (2020) Rhizosphere microbiome: Engineering bacterial competitiveness for enhancing crop production. J Adv Res 24:337–352. https://doi.org/10.1016/j.jare.2020.04.014
Kumar RK, Abhishek Mathur, Garima Awasthi, Kumud Kant Awasthi (2023) Actinobacteria as biological nitrogen fixation (BNF) and symbiotic association with actinorhizal plants for restoration of salinized soils. Materials Today: Proceedings. https://doi.org/10.1016/j.matpr.2023.07.143
Kumari S, Deepak Kumar, Paul Khurana SM (2022) Microbial degradation of pesticides: microbial potential for degradation of pesticides. In: Shah MP, Susana Rodriguez-Couto, Riti Thapar Kapoor (eds) Development in Wastewater Treatment Research and Processes, pp. 41–67, https://doi.org/10.1016/B978-0-323-85657-7.00005-5
Laplaze L, Gherbi H, Frutz T, Pawlowski K, Franche C, Macheix JJ, Auguy F, Bogusz D, Duhoux E (1999) Flavan-containing cells delimit Frankia-infected compartments in Casuarina glauca nodules. Plant Physiol 121:113–122. https://doi.org/10.1104/pp.121.1.113
Lefrançois E, Quoreshi A, Khasa D, Fung M, Whyte LG, Roy S, Greer CW (2010) Field performance of alder-Frankia symbionts for the reclamation of oil sands sites. Appl Soil Ecol 46(2):183–191. https://doi.org/10.1016/j.apsoil.2010.08.010
Lehnert N, Dong HT, Harland JB et al (2018) Reversing Nitrogen Fixation Nat Rev Chem 2:278–289. https://doi.org/10.1038/s41570-018-0041-7
Li CY, Strzelczyk E (2000) Belowground microbial processes underpin forest productivity. Phyton 40:129–134
Li SB, Xie ZZ, Hu CG, Zhang JZ (2016) A review of auxin response factors (ARFs) in plants. Front Plant Sci 7:47. https://doi.org/10.3389/fpls.2016.00047
Liu J, Bisseling T (2020) Evolution of NIN and NIN-like Genes in Relation to Nodule Symbiosis. Genes (basel) 11(7):777. https://doi.org/10.3390/genes11070777
Lopes MJS, Dias-Filho MB, Gurgel ESC (2021) Successful Plant Growth-Promoting Microbes: Inoculation Methods and Abiotic Factors. Front Sustain Food Syst 5:606454. https://doi.org/10.3389/fsufs.2021.606454
Lv L, Gao Z, Liao K, Zhu Q, Zhu J (2023) Impact of conservation tillage on the distribution of soil nutrients with depth. Soil Tillage Res 225:105527. https://doi.org/10.1016/j.still.2022.105527
Ma O-M, Carmen del Santoyo G (2021) Plant-microbial endophytes interactions: Scrutinizing their beneficial mechanisms from genomic explorations. Curr Plant Biol 25:100189. https://doi.org/10.1016/j.cpb.2020.100189
Malhi Y, Franklin J, Seddon N, Solan M, Turner MG, Field CB, Knowlton N (2020) Climate change and ecosystems: threats, opportunities and solutions. Philos Trans R Soc Lond B Biol Sci 375(1794):20190104. https://doi.org/10.1098/rstb.2019.0104
Manning WJ, Godzik B (2004) Bioindicator plants for ambient ozone in central and eastern Europe. Environ Pollut 130:330–339. https://doi.org/10.1016/j.envpol.2003.10.033
Mbengue MD, Christine Herve, Frederic Debelle (2020) Nod factor signaling in symbiotic nodulation. In: Pierre Frendo, Florian Frugier, Catherine Masson-Boivin (eds) Adv Bot Res. Academic Press, 94:1–39. https://doi.org/10.1016/bs.abr.2019.10.002
Yanthan M. Misra, AK (2013) Molecular approach to the classification of medicinally important actinorhizal genus Myrica. Ind J Biotechnol 12:133–136. https://api.semanticscholar.org
Misra AK, Sen A (2022) Frankia-The Endo-Micro-Symbiont of Hippophae Sp. In: Sharma PC (eds) The Seabuckthorn Genome. Compendium of Plant Genomes. Springer, Cham. https://doi.org/10.1007/978-3-031-11276-8_13
Mittermeier RA, Gil PR, Hoffmann M, Pilgrim J, Brooks T, Mittermeier CG, Lamoreux J, da Fonseca GAB (2004) Hotspots revisited: earth’s biologically richest and most threatened terrestrial ecoregions. Cemex, Cons Int, Agrupacion, Sierra Madre
Mohanram S, Kumar P (2019) Rhizosphere microbiome: revisiting the synergy of plant-microbe interactions. Ann Microbiol 69:307–320. https://doi.org/10.1007/s13213-019-01448-9
Molina R (1981) Ectomycorrhizal specificity in the genus Alnus. Can J Bot 59:325–334. https://doi.org/10.1139/b81-04
Mondal S, Suman Kumar Halder, Keshab Chandra Mondal (2022) Revisiting soil-plant-microbes interactions: Key factors for soil health and productivity. Soni R, Suyal DC, Yadav AN, Goel R (eds) In Developments in Applied Microbiology and Biotechnology. Trends Appl Microbiol Sust Econ. Academic Press, pp. 125–154. https://doi.org/10.1016/B978-0-323-91595-3.00022-7
Mortensen LM, Skre O (1990) Effects of low ozone concentrations on growth of Betula pubescens Ehrh., Betula verrucosa Ehrh. and Alnus incana (L.) Moench. New Phytol 115:165–170. https://doi.org/10.1111/j.1469-8137.1990.tb00934.x
Mounce R, Smith P, Brockington S (2017) Ex situ conservation of plant diversity in the world’s botanic gardens. Nature Plants 3:795–802. https://doi.org/10.1038/s41477-017-0019-3
Mus F, Hsin-Hua Wu (2022) Symbiotic nitrogen fixation. Ref Module Earth Sys Environ Sci. https://doi.org/10.1016/B978-0-12-822974-3.00056-2
Natesan S, Rajaram S, Manoharan D, Ramachandran T (2023) The Beneficial Plant Microbial Association for Sustainable Agriculture. In: Chhabra S, Prasad R, Maddela NR, Tuteja N (eds) Plant Microbiome Plant Produc Sust Agricult. Microorganisms for Sustainability vol 37. Springer, Singapore. https://doi.org/10.1007/978-981-19-5029-2_7
Nayar MP (1996) Hotspots of endemic plants of India, Nepal and Bhutan. TBGRI, Thiruvananthpuram, India
Nesic M, Bjedov I (2021) Habitat Degradation: Pressures, Threats, and Conservation. In: Leal Filho W, Azul AM, Brandli L, Lange Salvia A, Wall T (eds) Life on Land. Encyclopedia of the UN Sustainable Development Goals. Springer, Cham. https://doi.org/10.1007/978-3-319-95981-8_65
Ngom M, Oshone R, Diagne N et al (2016a) Tolerance to environmental stress by the nitrogen-fixing actinobacterium Frankia and its role in actinorhizal plants adaptation. Symbiosis 70:17–29. https://doi.org/10.1007/s13199-016-0396-9
Ngom M, Oshone R, Hurst IVS, Abebe-Akele F, Simpson S, Morris K, Sy MO, Champion A, Thomas WK, Tisa LS (2016b) Permanent draft genome sequence for Frankia sp. strain CeD, a nitrogen-fixing actinobacterium isolated from the root nodules of Casuarina equistifolia grown in Senegal. Genome Announc 4(2):e00265–16. https://doi.org/10.1128/genomeA.00265-16
Nguyen TV, Wibberg D, Battenberg K et al (2016) An assemblage of Frankia Cluster II strains from California contains the canonical nod genes and also the sulfotransferase gene nodH. BMC Genomics 17:796. https://doi.org/10.1186/s12864-016-3140-1
Nguyen TV, Wibberg D, Vigil-Stenman T, Berckx F, Battenberg K et al (2019) Frankia-Enriched Metagenomes from the Earliest Diverging Symbiotic Frankia Cluster: They Come in Teams. Genome Biol Evol 11(8):2273–2291. https://doi.org/10.1093/gbe/evz153
Van Nguyen T, Pawlowski K (2017) Frankia and Actinorhizal Plants: Symbiotic Nitrogen Fixation. In: Mehna S (eds) Rhizotrophs: Plant Growth Promotion to Bioremediation. Microorganisms for Sustainability, vol 2. Springer, Singapore. https://doi.org/10.1007/978-981-10-4862-3_12
Niemann J, Tisa LS (2008) Nitric oxide and oxygen regulate truncated hemoglobin gene expression in Frankia strain CcI3. J Bacteriol 190:7864–7867. https://doi.org/10.1128/JB.01100-08
Nigro D, Fortunato S, Giove SL, Mazzucotelli E, Gadaleta A (2020) Functional Validation of Glutaminesynthetase and Glutamatesynthase Genes in Durum Wheat near Isogenic Lines with QTL for High GPC. Int J Mol Sci 21(23):9253. https://doi.org/10.3390/ijms21239253
Normand N, Nouioui I, Pujic P, Fournier P, Dubost A, Klenk HP et al (2018) Frankia canadensis sp. nov., isolated from root nodules of Alnus incana subspecies rugosa growing in Canada. Int J EvolSyst Microbiol 68:3001–3011. https://doi.org/10.1099/ijsem.0.002939
Nouioui I, Ghodhbane-Gtari F, Montero-Calasanz MDC, Goker M, Meier-Kolthoff JP, Schumann P et al (2016) Proposal of a type strain for Frankia alni (Woronin 1866) Von Tubeuf 1895, emended description of Frankia alni, and recognition of Frankia casuarinae sp. nov. and Frankia elaeagni sp. nov. Int J Syst Evol Microbiol 66:5201–5210. https://doi.org/10.1099/ijsem.0.001496
Nouioui I, Ghodhbane-Gtari F, Montero-Calasanz MDC, Rohde M, Tisa LS, Gtari M et al (2017a) Frankia inefficax sp. nov., an actinobacterial endophyte inducing ineffective, non-nitrogen-fixing, root nodules on its actinorhizal host plants. Antonie Van Leeuwenhoek 110:313–320. https://doi.org/10.1007/s10482-016-0801-7
Nouioui I, Montero-Calasanz MDC, Ghodhbane-Gtari F, Rohde M, Tisa LS, Klenk HP et al (2017b) Frankia Discariae sp. nov.: an infective and effective microsymbiont isolated from the root nodule of Discaria trinervis. Arch Microbiol 199:641–647. https://doi.org/10.1007/s00203-017-1337-6
Nouioui I, Gueddou A, Ghodhbane-Gtari F, Rhode M, Klenk GM, HP, (2017c) Frankia asymbiotica sp. nov., a non-infective actinobacterium isolated from Morella californica root nodule. Int J SystEvol Microbiol 67:4897–4901. https://doi.org/10.1099/ijsem.0.002153
Nouioui I, Ghodhbane-Gtari F, Rhode M, Sangal V, Klenk HP, Gtari M (2018a) Frankia irregularis sp. nov., an actinobacterium unable to nodulate its original host, Casuarina equisetifolia, but effectively nodulates members of the actinorhizal Rhamnales. Int J Syst Evol Microbiol 68:2883–2914. https://doi.org/10.1099/ijsem.0.002914
Nouioui I, Ghodhbane-Gtari F, Klenk HP, Gtari M (2018b) Frankia saprophytica sp. nov. an atypical non-infective (Nod–) and non-nitrogen fixing (Fix–) actinobacterium isolated from Coriaria nepalensis root nodules. Int J Syst Evol Microbiol 68:1090–1095. https://doi.org/10.1099/ijsem.0.002633
Nouioui I, Ghodhbane-Gtari F, Jando M, Tisa LS, Klenk HP, Gtari M (2019a) Frankia torreyi sp. nov., the first actinobacterium of the genus Frankia Brunchorst, 1886, 174AL isolated in axenic culture. Antonie Van Leeuwenhoek 112:57–65. https://doi.org/10.1007/s10482-018-1131-8
Nouioui I, Cortes-albayay C, Carro L, Castro JF, Gtari M, Ghodhbane-Gtari F, Klenk H-P, Tisa LS, Sangal V, Goodfellow M (2019b) Genomic Insights into Plant-Growth-Promoting Potentialities of the Genus Frankia. Front Microbiol 10:1457. https://doi.org/10.3389/fmicb.2019.01457
Nouioui I, Gtari-G F, Jando M, Klenk HP, Gtari M (2023) Frankia colletiae sp. nov., a nitrogen-fixing actinobacterium isolated from Colletia cruciata. Int J Sys Evol Microbiol 73:1. https://doi.org/10.1099/ijsem.0.005656
Ogwu MC, Osawaru ME (2022) Traditional Methods of Plant Conservation for Sustainable Utilization and Development. In: Chibueze Izah S. (eds) Biodiversity in Africa: Potentials, Threats and Conservation. Sustainable Development and Biodiversity, vol 29. Springer, Singapore. https://doi.org/10.1007/978-981-19-3326-4_17
Okushima Y, Overvoorde PJ, Arima K et al (2005) Functional genomic analysis of the AUXIN RESPONSE FACTOR gene family members in Arabidopsis thaliana: unique and overlapping functions of ARF7 and ARF19. Plant Cell 17:444–463. https://doi.org/10.1105/tpc.104.028316
Olanrewaju OS, Babalola OO (2022) The rhizosphere microbial complex in plant health: A review of interaction dynamics. J Int Agric 21(8):2168–2182. https://doi.org/10.1016/S2095-3119(21)63817-0
Oshone R, Ngom M, Abebe-Akele F, Simpson S, Morris K, Sy MO, Champion A, Thomas WK, Tisa LS (2016) Permanent Draft Genome Sequence of Frankia sp. Strain Allo2, a Salt-Tolerant Nitrogen-Fixing Actinobacterium Isolated from the Root Nodules of Allocasuarina. Genome Announc 4(3):e00388–16. https://doi.org/10.1128/genomeA.00388-16
Oulhen N, Schulz BJ, Carrier TJ (2016) English translation of Heinrich Anton de Bary’s 1878 speech, ‘Die Erscheinung der Symbiose’ (‘De la symbiose’). Symbiosis 69:131–139. https://doi.org/10.1007/s13199-016-0409-8
Pan J, Huang C, Peng F, Zhang W, Luo J, Ma S, Xue X (2020) Effect of Arbuscular Mycorrhizal Fungi (AMF) and Plant Growth-Promoting Bacteria (PGPR) Inoculations on Elaeagnus angustifolia L. Saline Soil Appl Sci 10(3):945. https://doi.org/10.3390/app10030945
Periasamy S, Shanmugam RS (2022) Agricultural Land Degradation in India. In: Pereira P, Munoz-Rojas M, Bogunovic I, Zhao W (eds) Impact of Agriculture on Soil Degradation I. The Handbook of Environmental Chemistry, vol 120. Springer, Cham. https://doi.org/10.1007/698_2022_913
Persson T, Benson DR, Normand P, Vanden Heuvel B, Pujic P, Chertkov O et al (2011) Genome sequence of “Candidatus Frankia datiscae” Dg1, the uncultured microsymbiont from nitrogen-fixing root nodules of the dicot Datisca glomerata. J Bacteriol 193:7017–7018. https://doi.org/10.1128/JB.06208-11
Pii Y, Mimmo T, Tomasi N et al (2015) Microbial interactions in the rhizosphere: beneficial influences of plant growth-promoting rhizobacteria on nutrient acquisition process. A Review Biol Fertil Soils 51:403–415. https://doi.org/10.1007/s00374-015-0996-1
Pitts RJ, Cernac A, Estelle M (1998) Auxin and ethylene promote root hair elongation in Arabidopsis. The Plant J 16:553–560. https://doi.org/10.1046/j.1365-313x.1998.00321.x
Popovici J, Walker V, Bertrand CD, Bellvert F, Fernandez MP, Comte G (2011) Strain specificity in the Myricaceae-Frankia symbiosis is correlated to plant root phenolics. Funct Plant Biol 38(9):682–689. https://doi.org/10.1071/FP11144
Prakash R et al (2022) Rhizobacteriome: Plant Growth-Promoting Traits and Its Functional Mechanism in Plant Growth, Development, and Defenses. In: Veera Bramhachari P, (eds) Understanding the Microbiome Interactions in Agriculture and the Environment. Springer, Singapore. https://doi.org/10.1007/978-981-19-3696-8_16
Quilbe J, Montiel J, Arrighi J-F, Stougaard J (2022) Molecular Mechanisms of Intercellular Rhizobial Infection: Novel Findings of an Ancient Process. Front Plant Sci 13:922982. https://doi.org/10.3389/fpls.2022.922982
Quoreshi AM, Roy S, Greer CW, Beaudin J, McCurdy D, Khasa DP (2007) Inoculation of green alder (Alnus crispa) with Frankia-ectomycorrhizal fungal inoculant under commercial nursery production conditions. Nat Plants J 8(3):271–281. https://doi.org/10.2979/NPJ.2007.8.3.271
Rahman A, Hosokawa S, Oono Y, Amakawa T, Goto N, Tsurumi S (2002) Auxin and ethylene response interactions during Arabidopsis root hair development dissected by auxin influx modulators. Plant Physiol 130:1908–1917. https://doi.org/10.1104/pp.010546
Rajpurohit D, Jhang T (2015) In Situ and Ex Situ Conservation of Plant Genetic Resources and Traditional Knowledge. In: Salgotra R, Gupta B. (eds) Plant Genetic Resources and Traditional Knowledge for Food Security. Springer, Singapore. https://doi.org/10.1007/978-981-10-0060-7_8
Rascio N, La Rocca N (2013) Biological Nitrogen Fixation. Reference Module in Earth Systems and Environmental Sciences. https://doi.org/10.1016/B978-0-12-409548-9.09470-7
Rodgers WA, Panwar HS, Mathur VB (2000) Wildlife protected area network in India: a review. Wildlife Institute of India, Dehradun
Roy S, Khasa DP, Greer CW (2007) Combining alders, frankiae, and mycorrhizae for the revegetation and remediation of contaminated ecosystems. Can J Bot 85:237–251. https://doi.org/10.1139/B07-017
Saikia P, Kumar A, Khan ML (2016) Biodiversity Status and Climate Change Scenario in Northeast India. In: Nautiyal S, Schaldach R, Raju K, Kaechele H, Pritchard B, Rao K (eds) Climate Change Challenge (3C) and Social-Economic-Ecological Interface-Building. Environ Sci Eng. Springer, Cham. https://doi.org/10.1007/978-3-319-31014-5_8
Salgotra RK, Chauhan BS (2023) Genetic Diversity, Conservation, and Utilization of Plant Genetic Resources. Genes (basel) 14(1):174. https://doi.org/10.3390/genes14010174
Santi C et al (2013) Biological nitrogen fixation in non-legume plants. Ann Bot 111(5):743–767. https://doi.org/10.1093/aob/mct048
Santos CL, Vieira J, Sellstedt A, Normand P, Moradas-Ferreira P, Tavares F (2007) Modulation of Frankia alni ACN14a oxidative stress response: activity, expression and phylogeny of catalases. Physiol Plant 130:454–463. https://doi.org/10.1111/j.1399-3054.2007.00868.x
Santoyo G, Guzman-Guzman P, Parra-Cota FI, Sdl S-V, Orozco-Mosqueda MdC, Glick BR (2021) Plant Growth Stimulation by Microbial Consortia. Agronomy 11(2):219. https://doi.org/10.3390/agronomy11020219
Sarasan V, Cripps R, Ramsay MM, Atherton C, McMichen M, Prendergast G, Rowntree JK (2006) Conservation in vitro of threatened plants-progress in the past decade. In Vitro Cell Dev Biol Plant 42:206–214. https://doi.org/10.1079/IVP2006769
Sarubbo LA, Maria da Gloria C, Silva IJ, Durval B, Karen Gercyane O (2022) Biosurfactants: Production, properties, applications, trends, and general perspectives. Biochem Eng J 181:108377. https://doi.org/10.1016/j.bej.2022.108377
Sasakura F, Uchiumi T, Shimoda Y, Suzuki A, Takenouchi K, Higashi S, Abe M (2006) A class 1 hemoglobin gene from Alnus firma functions in symbiotic and nonsymbiotic tissues to detoxify nitric oxide. Mol Plant Microbe Interact 19:441–450. https://doi.org/10.1094/MPMI-19-0441
Sayed WF (2011) Improving Casuarina growth and symbiosis with Frankia under different soil and environmental conditions-review. Folia Microbiol 56:1–9. https://doi.org/10.1007/s12223-011-0002-8
Scaria SS, Lokesh Ravi (2023) Symbiotic associations of Frankia in actinorhizal plants. In: Dhanasekaran D (eds) Developments in Appl Microbiol Biotechnol. Microbial Symbionts, Academic Press, pp. 397–416. https://doi.org/10.1016/B978-0-323-99334-0.00002-5
Schroeter SA, Eveillard D, Chaffron S et al (2022) Microbial community functioning during plant litter decomposition. Sci Rep 12:7451. https://doi.org/10.1038/s41598-022-11485-1
Sharma S, Chhabra M, Singh SK et al. (2022) Genetic diversity and population structure of critically endangered Dactylorhiza hatagirea (D. Don) Soo from North-Western Himalayas and implications for conservation. Sci Rep 12, 11699. https://doi.org/10.1038/s41598-022-15742-1
Siddiqui H, Singh P, Arif Y, Sami F, Naaz R, Hayat S (2022) Role of Micronutrients in Providing Abiotic Stress Tolerance. In: Khan ST, Malik A (eds) Microbial Biofertilizers and Micronutrient Availability. Springer, Cham. https://doi.org/10.1007/978-3-030-76609-2_6
Silva LCR, Lambers H (2021) Soil-plant-atmosphere interactions: structure, function, and predictive scaling for climate change mitigation. Plant Soil 461:5–27. https://doi.org/10.1007/s11104-020-04427-1
Singh A, Mishra AK, Singh SS, Sarma HK, Shukla E (2008) Influence of iron and chelator on siderophore production in Frankia strains nodulating Hippophae salicifolia D. Don J Basic Microbiol 48:104–111. https://doi.org/10.1002/jobm.200700262
Singh K, Gupta K, Tyagi V, Rajkumar S. (2020) Plant genetic resources in India: management and utilization. Vavilovskii Zhurnal Genet Selektsii. 24(3):306–314. https://doi.org/10.18699/VJ20.622
Sokol NW, Slessarev E, Marschmann GL et al (2020) Life and death in the soil microbiome: how ecological processes influence biogeochemistry. Nat Rev Microbiol 20:415–430. https://doi.org/10.1038/s41579-022-00695-z
Strassburg BBN, Iribarrem A, Beyer HL et al (2020) Global priority areas for ecosystem restoration. Nature 586:724–729. https://doi.org/10.1038/s41586-020-2784-9
Sugiyama A (2021) Flavonoids and saponins in plant rhizospheres: roles, dynamics, and the potential for agriculture. Biosci Biotechnol Biochem 85(9):1919–1931. https://doi.org/10.1093/bbb/zbab106
Svistoonoff S, Hocher V, Gherbi H (2014) Actinorhizal root nodule symbioses: what is signalling telling on the origins of nodulation? Curr Opin Plant Biol 20:11–18. https://doi.org/10.1016/j.pbi.2014.03.001
Szczyglowski K, Ross L (2021) Baring the roots of nodulation. Nat Plants 7:244–245. https://doi.org/10.1038/s41477-021-00886-1
Temperton VM, Grayston SJ, Jackson G, Barton CVM, Millard P, Jarvis PG (2003) Effects of elevated carbon dioxide concentration on growth and nitrogen fixation in Alnus glutinosa in a long-term field experiment. Tree Physiol 23:1051–1059. https://doi.org/10.1093/treephys/23.15.1051
Thirugnanam T, Dhanasekaran Dharumadurai, Balasubramani Rajan, Udhayasuriyan Perachiselvi (2023) Symbiotic functional molecules in endophytic actinobacteria in actinorhizal plants: scientometric profile. In: Dharumadurai D (eds) Dev Appl Microbiol Biotechnol, Microbial Symbionts, Academic Press, pp. 235–261. https://doi.org/10.1016/B978-0-323-99334-0.00043-8
Tisa LS, Oshone R, Sarkar I, Ktari A, Sen A, Gtari M (2016) Genomic approaches toward understanding the actinorhizal symbiosis: an update on the status of the Frankia genomes. Symbiosis 70:5–16. https://doi.org/10.1007/s13199-016-0390-2
Tobita H, Uemura A, Kitao M, Kitaoka S, Utsugi H (2010) Interactive effects of elevated CO2, phosphorus deficiency, and soil drought on nodulation and nitrogenase activity in Alnus hirsuta and Alnus maximowiczii. Symbiosis 50:59–69. https://doi.org/10.1007/s13199-009-0037-7
Tobita H, Yazaki K, Harayama H et al (2016) Responses of symbiotic N2 fixation in Alnus species to the projected elevated CO2 environment. Trees 30:523–537. https://doi.org/10.1007/s00468-015-1297-x
Tokas D, Singh S, Yadav R, Singh AN (2023) Plant-microbe interactions: Role in sustainable agriculture and food security in a changing climate. In: Swapnil P, Mukesh Meena, Harish, Avinash Marwal, Selvakumar Vijayalakshmi, Andleeb Zehra (eds), Plant-Microbe Interaction-Recent Advances in Molecular and Biochemical Approaches, Academic Press, pp. 363–391. https://doi.org/10.1016/B978-0-323-91876-3.00008-7
Trivedi P, Leach JE, Tringe SG et al (2020) Plant-microbiome interactions: from community assembly to plant health. Nat Rev Microbiol 18:607–621. https://doi.org/10.1038/s41579-020-0412-1
Tsai HH, Schmidt W (2021) The enigma of environmental pH sensing in plants. Nat Plants 7:106–115. https://doi.org/10.1038/s41477-020-00831-8
Veerapagu M, Ashraf Khalifa, Jeya KR, Sankaranarayanan A (2023) Frankia from actinorhizal plants. In: Dhanasekaran D (eds) Dev Appl Microbiol Biotechnol. Microbial Symbionts. Academic Press, pp. 57–74. https://doi.org/10.1016/B978-0-323-99334-0.00026-8
Velmourougane K, Saxena G, Prasanna R (2017) Plant-Microbe Interactions in the Rhizosphere: Mechanisms and Their Ecological Benefits. In: Singh D, Singh H, Prabha R (eds) Plant-Microbe Interactions in Agro-Ecological Perspectives. Springer, Singapore. https://doi.org/10.1007/978-981-10-6593-4_7
Vemulapally S, Guerra T, Hahn D (2019) Localization of typical and atypical Frankia isolates from Casuarina sp. in nodules formed on Casuarina equisetifolia. Plant and Soil 435(1/2):385–393. https://www.jstor.org/stable/48703686
Venkataraman K, Sivaperuman C. (2018) Biodiversity Hotspots in India. In: Sivaperuman C, Venkataraman K. (eds) Indian Hotspots. Springer, Singapore. https://doi.org/10.1007/978-981-10-6605-4_1
Venkataraman K, Sivaperuman C (2018) Biodiversity Hotspots in India. In: Sivaperuman C, Venkataraman K (eds) Indian Hotspots. Springer, Singapore. https://doi.org/10.1007/978-981-10-6605-4_1
Vincent M, Boubakri H, Gasser M et al (2023) What contribution of plant immune responses in Alnus glutinosa-Frankia symbiotic interactions? Symbiosis 89:27–52. https://doi.org/10.1007/s13199-022-00889-2
Vissenberg K et al (2020) Hormonal regulation of root hair growth and responses to the environment in Arabidopsis. J Exp Bot 71(8):2412–2427. https://doi.org/10.1093/jxb/eraa048
Vives-Peris V, de Ollas C, Gomez-Cadenas A et al (2020) Root exudates: from plant to rhizosphere and beyond. Plant Cell Rep 39:3–17. https://doi.org/10.1007/s00299-019-02447-5
Vogel CS, Curtis PS, Thomas RB (1997) Growth and nitrogen accretion of dinitrogen-fixing Alnus glutinosa (L.) Gaertn. under elevated carbon dioxide. Plant Ecol 130:63–70. https://doi.org/10.1023/A:1009783625188
Vostinar AE, Skocelas KG, Lalejini A, Zaman L (2021) Symbiosis in Digital Evolution: Past, Present, and Future. Front Ecol Evol 9:739047. https://doi.org/10.3389/fevo.2021.739047
Watanabe Y, Tobita H, Kitao M, Maruyama Y, Choi D, Sasa K, Funada R, Koike T (2008) Effects of elevated CO2 and nitrogen on wood structure related to water transport in seedlings of two deciduous broad-leaved tree species. Trees 22:403–411. https://doi.org/10.1007/s00468-007-0201-8
Wheeler CT, Hughes LT, Oldroyd J, Pulford ID (2001) Effects of nickel on Frankia and its symbiosis with Alnus glutinosa (L.) Gaertn. Plant Soil 231:81–90. https://doi.org/10.1023/A:1010304614992
Wheeler C, Akkermans A, Berry A (2008) Frankia and Actinorhizal Plants: A Historical Perspective. In: Pawlowski K, Newton WE (eds) Nitrogen-fixing Actinorhizal Symbioses. Nitrogen Fixation: Origins, Applications, and Research Progress, vol 6. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-3547-0_1
Wolfe ER, Singleton S, Stewart NU et al (2022) Frankia diversity in sympatrically occurring red alder (Alnus rubra) and Sitka alder (Alnus viridis) trees in an early successional environment. Trees 36:1665–1675. https://doi.org/10.1007/s00468-022-02317-w
Xun W, Shao J, Shen Q, Zhang R (2021) Rhizosphere microbiome. Functional compensatory assembly for plant fitness. Comput Struct Biotechnol J 19:5487–5493. https://doi.org/10.1016/j.csbj.2021.09.035
Yamanaka T, Li CY, Bormann BT, Okabe H (2003a) Tripartite associations in an alder: effects of Frankia and Alpova diplophloeus on the growth, nitrogen fixation and mineral acquisition of Alnus tenuifolia. Plant Soil 254:179–186. https://doi.org/10.1023/A:1024938712822
Yamanaka T, Li CY, Bormann BT, Okabe H (2003b) Tripartite associations in an alder: effects of Frankia and Alpova diplophloeus on the growth, nitrogen fixation and mineral acquisition of Alnus tenuifolia. In: Normand P, Dawson JO, Pawlowski K (eds) Frankia Symbiosis. Developments in Plant and Soil Sciences, vol 100. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-1601-7_19
Yaynemsa KG (2022) Anthropogenic Impact on Plant Biodiversity. In: Plant Biodiversity Conservation in Ethiopia. Springer, Cham. https://doi.org/10.1007/978-3-031-20225-4_2
Ye JY, Tian WH, Jin CW (2022) Nitrogen in plants: from nutrition to the modulation of abiotic stress adaptation. Stress Biology 2:4. https://doi.org/10.1007/s44154-021-00030-1
Zachar I, Boza G (2020) Endosymbiosis before eukaryotes: mitochondrial establishment in protoeukaryotes. Cell Mol Life Sci 77(18):3503–3523. https://doi.org/10.1007/s00018-020-03462-6
Zhang L, Huang Y, Rong L et al (2021) Effect of soil erosion depth on crop yield based on topsoil removal method: a meta-analysis. Agron Sustain Dev 41:63. https://doi.org/10.1007/s13593-021-00718-8
Zhou X, Tian L, Zhang J, Ma L, Li X, Tian C (2017) Rhizospheric fungi and their link with the nitrogen-fixing Frankia harbored in host plant Hippophae rhamnoides L. J Basic Microbiol 57(12):1055–1064. https://doi.org/10.1002/jobm.201700312
Acknowledgements
For logistics and support, the authors thank the Principal, NNS College, Titabar, Jorhat, Assam, India. PNB and NFI also appreciated the Department of Biotechnology, Govt. of India, for granting research funds for Institutional Biotech Hub (BT/NER/143/SP44344/2021) at NNS College, under NER Biotech Hub Programme.
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PNB: Conception and design of the research, initial data collection and compilation, analysis and interpretation of data and preparation of the original draft, revised, formatted and submission.
NFI: Revised the original manuscript, data collection, and formatted.
BS: Data collection and assisted in the preparation of the original draft, revised and formatted.
BCN: Revised the original draft and formatted.
LKTAA: Revised the original draft and data validation.
DL: Revised the original draft and formatted.
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Bhattacharyya, P.N., Islam, N.F., Sarma, B. et al. Frankia-actinorhizal symbiosis: a non-chemical biological assemblage for enhanced plant growth, nodulation and reclamation of degraded soils. Symbiosis 92, 1–26 (2024). https://doi.org/10.1007/s13199-023-00956-2
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DOI: https://doi.org/10.1007/s13199-023-00956-2