Cordia africana but not Juniperus procera and Podocarpus falcatus respond positively to arbuscular mycorrhizal fungi at the early stages of seedling development
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Abstract. Asmelash F, Bekele T, Belay Z, Kebede F. 2021. Cordia africana but not Juniperus procera and Podocarpus falcatus respond positively to arbuscular mycorrhizal fungi at the early stages of seedling development. Biodiversitas 22: 2971-2980. AMF (Arbuscular mycorrhizal fungi) inoculation could be an important technology to improve the growth and field survival of trees. Hence, we evaluated the mycorrhizal responsiveness of Cordia africana Lam., Juniperus procera (Hoechst. ex Endl.), and Podocarpus falcatus (Thumb.) Mirb. seedlings. Seedlings germinated on sterile sand were transplanted to 1-liter plastic pots filled with sterile and non-sterile degraded bulk soil. Rhizospheric soil from adult C. africana and J. procera were used as whole-soil AMF inocula. Cordia africana and J. procera received conspecific whole-soil AMF inocula while P. falcatus received J. procera inoculum. Hence, in the two-by-two factorial experiment, we also evaluated the growth effects of AMF inoculation, soil type, and their interaction. On the sterile potting soil, MRi (mycorrhizal responsiveness due to AMF inoculation) of C. africana was positive and significantly (p<0.05) greater than the MRi of J. procera and P. falcatus. However, on the non-sterile potting soil, it was significantly greater than the MRi of P. falcatus only. MRs (MR due to the existing potting soil inocula) and considering all growth variables were mostly positive for C. africana but negative for J. procera and P. falcatus. AMF inoculation significantly increased most growth variables of C. africana seedlings and no significant “inoculation” x “soil type” interaction effects were detected. Hence, AMF inoculation of C. africana seedlings could be merited and under wide range of field conditions. In the case of J. procera and P. falcatus, after-planting care could be more appropriate
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References
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Asmelash F, Bekele T, Birhane E. 2016. The potential role of arbuscular mycorrhizal fungi in the restoration of degraded lands. Front Microbiol 7:1095
Asmelash F, Bekele T, Belay, Z. 2019. Comparative field survival and growth of selected Ethiopian native tree species and the effect of whole soil AMF inoculation. J. Hort. For. 11:19–31.
Asmelash, F., Bekele, T., Kebede, F., and Belay, Z. (2020). The arbuscular mycorrhizal fungi status of selected tree nurseries in the Ethiopian highlands. J. For. Res. https://doi.org/10.1007/s11676-020-01169-9
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Baylis GTS, McNabb RFR, Morrison TM. 1963. The mycorrhizal nodules of Podocarps. Trans. Brit. Mycol. Soc. 46 (3):378–384.
Bishaw B. 2001. Deforestation and land degradation in the Ethiopian highlands: A strategy for physical recovery. Northeast Afri. Stud. 8:7–26.
Carrillo-Garcial A, Leon de la Luz J-L, Bashan Y, Bethlenfalvay GJ. 1999. Nurse plants, mycorrhizae, and plant establishment in a disturbed area of the Sonoran desert. Restor. Ecol. 7:321–335.
Comas LH, Becker SR, Cruz VMV, Byrne PF, Dierig DA. 2013. Root traits contributing to plant productivity under drought. Front. Plan. Sci. 4:1-16.
Dalling JW, Heineman K, González G, Ostertag R. 2016. Geographic, environmental and biotic sources of variation in the nutrient relations of tropical montane forests. J. Trop. Ecol. 32:368–383.
Dobo B, Asefa F, Asfaw Z. 2016. Response of Selected Perennial Crops and Trees to AMF Inoculation and NPK Application in Pot Culture. Aca. J. Biotech. 4:325–336.
Duponnois R, Ouahmane L, Kane A, Thioulouse J, Hafidi M, Boumezzough A, Prin Y, Baudoin, E, Galiana A, Dreyfus B. 2011. Nurse shrubs increased the early growth of Cupressus seedlings by enhancing belowground mutualism and soil microbial activity. Soil Biol. Biochem. 43:2160–2168.
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Gavito ME, Perez-Castillo D, Gonzalez-Monterrubio C, Vieyra-Hernandez MT, Martínez-Trujillo M. 2008. High compatibility between arbuscular mycorrhizal fungal communities and seedlings of different land use types in a tropical dry ecosystem. Mycor. 19:47–60.
Giovanetti M, Mosse, B. 1980. An evaluation of techniques for measuring vesicular arbuscularmycorrhizal infection in roots. New Phytol. 84:489–500.
Gutjahr C. 2014. Phytohormone signalling in arbuscular mycorrhiza development. Curr. Opin. Plant Biol., 20: 26–34. doi:10.1016/j.pbi.2014.04.003
Hart MM, Reader RJ. 2004. Do arbuscular mycorrhizal fungi recover from soil disturbance differently? Trop. Ecol. 45:97–111
Huante P, Ceccon E, Orozco-Segovia A, Sánchez-Coronado ME, Acosta I, Rincón, E. 2012. The role of arbuscular mycorrhizal fungi on the early stage restoration of seasonally dry tropical rain forest in Chamela, Mexico. Revi. Árv. Viçosa-MG. 36:279–289.
Hunt, R. 1990. Basic Growth Analysis: Plant growth analysis for beginners. Unwin Hyman Ltd, UK.
Janos DP. 2007. Plant responsiveness to mycorrhizas differs from dependence upon mycorrhizas. Mycor. 17:75–91.
Kiers ET, Lovelock CE, Krueger EL, Herre EA. 2000. Differential effects of tropical arbuscular mycorrhizal fungal inocula on root colonization and tree seedling growth: implications for tropical forest diversity. Ecol. Let. 3:106–113.
Leake J, Johnson D, Donnelly D, Muckle G, Boddy L, Read D. 2004. Networks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning. Can. J. Bot, 82:1016–1045.doi: 10.1139/B04-060
Lemenih M, Teketay, D. 2004. Restoration of native forest flora in the degraded highlands of ethiopia: constraints and opportunities. SINET 27:75–90.
Michelsen A (1992) Mycorrhiza and root nodulation in tree seedlings from five nurseries in Ethiopia and Somalia. For Ecol Manag 48:335–344
Muleta D. 2017. Legume Response to Arbuscular Mycorrhizal Fungi Inoculation in Sustainable Agriculture. In: Microbes for Legume Improvement, 2nd ed., pp. 227-260 (Khan, M.S., Zaidi, A. and Musarrat, J., eds.). Springer International Publishing
Negash L. 2010. A Selection of Ethiopia's Indigenous Trees: Biology, Uses and Propagation Techniques. Addis Ababa University Press, Addis Ababa, Ethiopia.
Onguene NA, Kuyper TW. 2005. Growth response of three native timber species to soils with different arbuscular mycorrhizal inoculums potentials in South Cameroon Indigenous inoculum and effect of addition of grass inoculums. For. Ecol. Man. 210:283–290.
Ouahmane L, Hafidi M, Kisa M, Boumezzough A, Thoulouse J, Duponnois R. 2006. Lavandula species as accompanying plants in Cupressus replanting strategies: effect on plant growth, mycorrhizal soil infectivity and soil microbial catabolic diversity. Appl. Soil & Ecol. 34:90–199.
Pandey SK, Singh H. 2011. A simple, cost-effective method for leaf area estimation. J. Bot. Article ID 658240:1–6.
Pánková H, Münzbergová Z, Rydlová J, Vosátka M. 2014. Co-Adaptation of Plants and Communities of Arbuscular Mycorrhizal Fungi to Their Soil Conditions. Fol. Geob. 49:521–540.
Rowe HI, Brown CY, Claassen VP. 2007. Comparisons of Mycorrhizal Responsiveness with Field Soil and Commercial Inoculum for Six Native Montane Species and Bromus tectorum. Restor. Ecol. 15:44–52.
Russell AJ, Bidartondo MI, Butterfield BG. 2002. The root nodules of the Podocarpaceae harbor arbuscular mycorrhizal fungi. New Phytol. 156: 283–295
Schüßler A, Krüger C, Urgiles N. 2016. Phylogenetically diverse AM fungi from Ecuador strongly improve seedling growth of native potential crop trees. Mycor. 26:199–207
Smith SE, Read DJ. 2008. Mycorrhizal Symbiosis, 3rd edn. Academic Press, Cambridge, p 800
Strassburg, BBN, Iribarrem A, Beyer HL, Cordeiro CL, Crouzeilles R, Jakovac CC, Junqueira AB, Lacerda E, Latawiec AE, Balmford A, Brooks TM, Butchart SHM, Chazdon RL, Erb K-H, Brancalion P, Buchanan G, Cooper D, Díaz S, Donald PF, Kapos V, Leclère D, Miles L, Obersteiner M, Plutzar C, Scaramuzza CA, deM, Scarano FR, Visconti P. (2020). Global priority areas for ecosystem restoration. Nature. Doi:10.1038/s41586-020-2784-9
Teketay D. 1997. Seedling populations and regeneration of woody species in dry Afromontane forests of Ethiopia. For. Ecol. Man. 98:149–165.
Verbruggen E, van der Heijden MGA, Rillig MC, Kiers ET (2013) Mycorrhizal fungal establishment in agricultural soils: factors determining inoculation success. New phytol 197(4):1104–1109
Vierheilig H, Coughlan AP, Wyss U, Piche Y. 1998. Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl. Env. Microb. 64:5004–5007.
Wubet T, Weiß M, Kottke I, Oberwinkler F. 2006. Two threatened coexisting indigenous conifer species in the dry Afromontane forests of Ethiopia are associated with distinct arbuscular mycorrhizal communities. Can. J. Bot. 84:1617–1627.
Yirdaw E, Leinonen K. 2002. Seed germination responses of four afromontane tree species to red/far-red ratio and temperature. For. Ecol. Man. 168:53–61.
Zangaro W, Bononi VLR, Trufem SFB. 2000. Mycorrhizal dependency, inoculum potential and habitat preference of native woody species in South Brazil. J. Trop. Ecol. 16:603–621.
Zangaro W, Nishidate FR, Vandresen J, Andrade G, Nogueira MN. 2007. Root mycorrhizal colonization and plant responsiveness are related to root plasticity, soil fertility and successional status of native woody species in southern Brazil. J. Trop. Ecol. 23:53–62.
Zangaro W, Nisizaki SMA, Domingos JCB, Nakano EM. 2003. Mycorrhizal response and successional status in 80 woody species from South Brazil. J. Trop. Ecol. 19:315–324.
Zarik L, Meddich A, Hijri M, Hafidi M, Ouhammoua A, Ouahmane L, Duponnois R, Boumezzough, A. (2016). Use of arbuscular mycorrhizal fungi to improve the drought tolerance of Cupressus atlantica G. Comptes Rendus Biologies. C. R. Biolog. 339:185–196.
Aerts R, Negussie N, Maes W, November E, Hermy M, Muys, B. 2007. Restoration of Dry Afromontane Forest Using Pioneer Shrubs as Nurse-Plants for Olea europaea ssp. cuspidata. Restor. Ecol. 15:129–138.
Asmelash F, Bekele T, Birhane E. 2016. The potential role of arbuscular mycorrhizal fungi in the restoration of degraded lands. Front Microbiol 7:1095
Asmelash F, Bekele T, Belay, Z. 2019. Comparative field survival and growth of selected Ethiopian native tree species and the effect of whole soil AMF inoculation. J. Hort. For. 11:19–31.
Asmelash, F., Bekele, T., Kebede, F., and Belay, Z. (2020). The arbuscular mycorrhizal fungi status of selected tree nurseries in the Ethiopian highlands. J. For. Res. https://doi.org/10.1007/s11676-020-01169-9
Barea JM, Palenzuela J, Cornejo P, Sánchez-Castro I, Navarro-Fernández C, Lopéz-García A, Estrada B, Azcón R, Ferrol N, Azcón-Aguilar C. 2011. Ecological and functional roles of mycorrhizas in semi-arid ecosystems of Southeast Spain. J. Ari. Env. 75:1292–1301.
Baylis GTS, McNabb RFR, Morrison TM. 1963. The mycorrhizal nodules of Podocarps. Trans. Brit. Mycol. Soc. 46 (3):378–384.
Bishaw B. 2001. Deforestation and land degradation in the Ethiopian highlands: A strategy for physical recovery. Northeast Afri. Stud. 8:7–26.
Carrillo-Garcial A, Leon de la Luz J-L, Bashan Y, Bethlenfalvay GJ. 1999. Nurse plants, mycorrhizae, and plant establishment in a disturbed area of the Sonoran desert. Restor. Ecol. 7:321–335.
Comas LH, Becker SR, Cruz VMV, Byrne PF, Dierig DA. 2013. Root traits contributing to plant productivity under drought. Front. Plan. Sci. 4:1-16.
Dalling JW, Heineman K, González G, Ostertag R. 2016. Geographic, environmental and biotic sources of variation in the nutrient relations of tropical montane forests. J. Trop. Ecol. 32:368–383.
Dobo B, Asefa F, Asfaw Z. 2016. Response of Selected Perennial Crops and Trees to AMF Inoculation and NPK Application in Pot Culture. Aca. J. Biotech. 4:325–336.
Duponnois R, Ouahmane L, Kane A, Thioulouse J, Hafidi M, Boumezzough A, Prin Y, Baudoin, E, Galiana A, Dreyfus B. 2011. Nurse shrubs increased the early growth of Cupressus seedlings by enhancing belowground mutualism and soil microbial activity. Soil Biol. Biochem. 43:2160–2168.
Friis I. 1992. Forests and forest trees of North-East Tropical Africa. Kew Bulletin Additional Series XV. HMSO. London.
Friis I, Demissew, D, Breugel PV. 2010. Atlas of the potential vegetation of Ethiopia. The Royal Danish Academy of Sciences, Biol Skrif 58, Denmark.
Gavito ME, Perez-Castillo D, Gonzalez-Monterrubio C, Vieyra-Hernandez MT, Martínez-Trujillo M. 2008. High compatibility between arbuscular mycorrhizal fungal communities and seedlings of different land use types in a tropical dry ecosystem. Mycor. 19:47–60.
Giovanetti M, Mosse, B. 1980. An evaluation of techniques for measuring vesicular arbuscularmycorrhizal infection in roots. New Phytol. 84:489–500.
Gutjahr C. 2014. Phytohormone signalling in arbuscular mycorrhiza development. Curr. Opin. Plant Biol., 20: 26–34. doi:10.1016/j.pbi.2014.04.003
Hart MM, Reader RJ. 2004. Do arbuscular mycorrhizal fungi recover from soil disturbance differently? Trop. Ecol. 45:97–111
Huante P, Ceccon E, Orozco-Segovia A, Sánchez-Coronado ME, Acosta I, Rincón, E. 2012. The role of arbuscular mycorrhizal fungi on the early stage restoration of seasonally dry tropical rain forest in Chamela, Mexico. Revi. Árv. Viçosa-MG. 36:279–289.
Hunt, R. 1990. Basic Growth Analysis: Plant growth analysis for beginners. Unwin Hyman Ltd, UK.
Janos DP. 2007. Plant responsiveness to mycorrhizas differs from dependence upon mycorrhizas. Mycor. 17:75–91.
Kiers ET, Lovelock CE, Krueger EL, Herre EA. 2000. Differential effects of tropical arbuscular mycorrhizal fungal inocula on root colonization and tree seedling growth: implications for tropical forest diversity. Ecol. Let. 3:106–113.
Leake J, Johnson D, Donnelly D, Muckle G, Boddy L, Read D. 2004. Networks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning. Can. J. Bot, 82:1016–1045.doi: 10.1139/B04-060
Lemenih M, Teketay, D. 2004. Restoration of native forest flora in the degraded highlands of ethiopia: constraints and opportunities. SINET 27:75–90.
Michelsen A (1992) Mycorrhiza and root nodulation in tree seedlings from five nurseries in Ethiopia and Somalia. For Ecol Manag 48:335–344
Muleta D. 2017. Legume Response to Arbuscular Mycorrhizal Fungi Inoculation in Sustainable Agriculture. In: Microbes for Legume Improvement, 2nd ed., pp. 227-260 (Khan, M.S., Zaidi, A. and Musarrat, J., eds.). Springer International Publishing
Negash L. 2010. A Selection of Ethiopia's Indigenous Trees: Biology, Uses and Propagation Techniques. Addis Ababa University Press, Addis Ababa, Ethiopia.
Onguene NA, Kuyper TW. 2005. Growth response of three native timber species to soils with different arbuscular mycorrhizal inoculums potentials in South Cameroon Indigenous inoculum and effect of addition of grass inoculums. For. Ecol. Man. 210:283–290.
Ouahmane L, Hafidi M, Kisa M, Boumezzough A, Thoulouse J, Duponnois R. 2006. Lavandula species as accompanying plants in Cupressus replanting strategies: effect on plant growth, mycorrhizal soil infectivity and soil microbial catabolic diversity. Appl. Soil & Ecol. 34:90–199.
Pandey SK, Singh H. 2011. A simple, cost-effective method for leaf area estimation. J. Bot. Article ID 658240:1–6.
Pánková H, Münzbergová Z, Rydlová J, Vosátka M. 2014. Co-Adaptation of Plants and Communities of Arbuscular Mycorrhizal Fungi to Their Soil Conditions. Fol. Geob. 49:521–540.
Rowe HI, Brown CY, Claassen VP. 2007. Comparisons of Mycorrhizal Responsiveness with Field Soil and Commercial Inoculum for Six Native Montane Species and Bromus tectorum. Restor. Ecol. 15:44–52.
Russell AJ, Bidartondo MI, Butterfield BG. 2002. The root nodules of the Podocarpaceae harbor arbuscular mycorrhizal fungi. New Phytol. 156: 283–295
Schüßler A, Krüger C, Urgiles N. 2016. Phylogenetically diverse AM fungi from Ecuador strongly improve seedling growth of native potential crop trees. Mycor. 26:199–207
Smith SE, Read DJ. 2008. Mycorrhizal Symbiosis, 3rd edn. Academic Press, Cambridge, p 800
Strassburg, BBN, Iribarrem A, Beyer HL, Cordeiro CL, Crouzeilles R, Jakovac CC, Junqueira AB, Lacerda E, Latawiec AE, Balmford A, Brooks TM, Butchart SHM, Chazdon RL, Erb K-H, Brancalion P, Buchanan G, Cooper D, Díaz S, Donald PF, Kapos V, Leclère D, Miles L, Obersteiner M, Plutzar C, Scaramuzza CA, deM, Scarano FR, Visconti P. (2020). Global priority areas for ecosystem restoration. Nature. Doi:10.1038/s41586-020-2784-9
Teketay D. 1997. Seedling populations and regeneration of woody species in dry Afromontane forests of Ethiopia. For. Ecol. Man. 98:149–165.
Verbruggen E, van der Heijden MGA, Rillig MC, Kiers ET (2013) Mycorrhizal fungal establishment in agricultural soils: factors determining inoculation success. New phytol 197(4):1104–1109
Vierheilig H, Coughlan AP, Wyss U, Piche Y. 1998. Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl. Env. Microb. 64:5004–5007.
Wubet T, Weiß M, Kottke I, Oberwinkler F. 2006. Two threatened coexisting indigenous conifer species in the dry Afromontane forests of Ethiopia are associated with distinct arbuscular mycorrhizal communities. Can. J. Bot. 84:1617–1627.
Yirdaw E, Leinonen K. 2002. Seed germination responses of four afromontane tree species to red/far-red ratio and temperature. For. Ecol. Man. 168:53–61.
Zangaro W, Bononi VLR, Trufem SFB. 2000. Mycorrhizal dependency, inoculum potential and habitat preference of native woody species in South Brazil. J. Trop. Ecol. 16:603–621.
Zangaro W, Nishidate FR, Vandresen J, Andrade G, Nogueira MN. 2007. Root mycorrhizal colonization and plant responsiveness are related to root plasticity, soil fertility and successional status of native woody species in southern Brazil. J. Trop. Ecol. 23:53–62.
Zangaro W, Nisizaki SMA, Domingos JCB, Nakano EM. 2003. Mycorrhizal response and successional status in 80 woody species from South Brazil. J. Trop. Ecol. 19:315–324.
Zarik L, Meddich A, Hijri M, Hafidi M, Ouhammoua A, Ouahmane L, Duponnois R, Boumezzough, A. (2016). Use of arbuscular mycorrhizal fungi to improve the drought tolerance of Cupressus atlantica G. Comptes Rendus Biologies. C. R. Biolog. 339:185–196.