Morpho-anatomical and molecular characterisation of ectomycorrhizae associated with Eucalyptus species growing in different areas of the Punjab Province, Pakistan
Hira Bashir A B and A. N. Khalid A
+ Author Affiliations
- Author Affiliations
A Department of Botany, University of the Punjab, New Campus, 54590, Lahore, Pakistan.
B Corresponding author. Email: hira.b21@hotmail.com
Australian Journal of Botany 62(8) 689-697 https://doi.org/10.1071/BT14095
Submitted: 2 June 2014 Accepted: 23 January 2015 Published: 26 March 2015
Abstract
An evaluation of the ectomycorrhizal status of Eucalyptus plantations in different areas of the Punjab Province, Pakistan is presented. Our study reveals a very low diversity of below-ground ectomycorrhizal fungi associated with Eucalyptus. Through molecular investigation, only three taxa were confirmed to be associated with six different species of Eucalyptus at four sampling sites. Among them, Scleroderma bovista was frequently associated with Eucalyptus in soils having different physicochemical properties highlighting wide ecological amplitude of this species. Scleroderma aurantium and Pisolithus tinctorius were infrequent associates with eucalypt roots. This study is the first consolidated approach to determine the ectomycorrhizal potential of exotic Eucalyptus with the innate fungal flora of Pakistan.
Additional keywords: amplification, Changa Manga Forest, dry temperate, ITS region, genome sequencing, morphotypes, RFLP.
References
Afshan N, Khalid AN, Niazi AR (2003) New ectomycorrhizas from Sakesar Hills. Mycopath 1, 100–104.Agerer R (1987–2012) ‘Color atlas of Ectomycorrhizae.’ (Einhorn-Verlag: Schwäbisch Gmünd)
Agerer R (1999) Anatomical characteristics of identified ectomycorrhizas: an attempt towards a natural classification. In ‘Mycorrhiza: structure, function, molecular biology and biotechnology’, 2nd edn. (Eds A Verma, B Hock) pp. 633–682. (Springer Verlag: Berlin)
Agerer R (2006) Fungal relationships and structural identity of their ectomycorrhizae. Mycological Progress 5, 67–107.
| Fungal relationships and structural identity of their ectomycorrhizae.Crossref | GoogleScholarGoogle Scholar |
Agerer R, Otto P (1997) Bankera fuligineo-alba (Schumidt, J. C. Fr.) Pouzar + Pinus sylvestris L. Descriptive Ectomycorrhizal 2, 1–6.
Ahmad S (1956) Fungi of Pakistan. Biological Society Pakistan Lahore. Monograph 1, 1–126.
Ahmad Z (2007) Country report on plant genetic resources for food and agriculture. Pakistan Agricultural Research Council, Islamabad, Pakistan
Ahmad A, Khan RA (1988) Rangeland development in Dera Ghazi Khan, Pakistan. Rangelands 10, 255–258.
Ahmed MT, Husain T, Sheikh AH, Hussain SS, Siddique MF (2006) Phytosociology and structure of Himalayan forests from different climatic zones of Pakistan. Pakistan Journal of Botany 38, 361–383.
Ashraf T, Hanif M, Khalid AN (2012) Peziza michelii and its ectomycorrhizae with Alnus nitida (Betulaceae) from Pakistan. Mycotaxon 120, 181–188.
| Peziza michelii and its ectomycorrhizae with Alnus nitida (Betulaceae) from Pakistan.Crossref | GoogleScholarGoogle Scholar |
Bakshi BK (1966) Mycorrhiza in eucalypts in India. Indian Forester 92, 19–20.
Bougher NL (1995) Diversity of ectomycorrhizal fungi associated with eucalpts in Australia. In ‘Mycorrhizas for plantation forestry in Asia – ACIAR Proceedings No. 6’. (Eds M Brundrett, B Dell, N Malajczuk, MQ Gongs) pp 28–15. (ACIAR: Canberra)
Bougher NL, Grove TS, Malajczuk N (1990) Growth and phosphorus acquisition of karri (Eucalyptus diversicolor F. Muell.) seedlings inoculated with ectomycorrhizal fungi in relation to phosphorus supply. New Phytologist 114, 77–85.
| Growth and phosphorus acquisition of karri (Eucalyptus diversicolor F. Muell.) seedlings inoculated with ectomycorrhizal fungi in relation to phosphorus supply.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXhslOntLc%3D&md5=fd6db2282eb9b2dc077404e0dd3624a1CAS |
Brundrett M, Bougher NL, Dell B, Grove G, Malajczuk N (1996) Working with mycorrhizas in forestry and agriculture. ACIAR Monograph 32 ACIAR, Canberra.
Bruns TD (1995) Thoughts on the processes that maintain local species diversity of ectomycorrhizal fungi. Plant and Soil 170, 63–73.
| Thoughts on the processes that maintain local species diversity of ectomycorrhizal fungi.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXlt1Kgtbg%3D&md5=386ab4e068635e247d0ed1519dc5fb13CAS |
Cairney JW, Chambers SM (1999) ‘Ectomycorrhizal fungi: key genera in profile.’ (Springer-Verlag: Berlin)
Chen YL, Brundrett MC, Dell B (2000a) Effects of ectomycorrhizas and vesicular-arbuscular mycorrhizas, alone or in competition, on root colonization and growth of Eucalyptus globulus and E. urophylla. New Phytologist 146, 545–555.
| Effects of ectomycorrhizas and vesicular-arbuscular mycorrhizas, alone or in competition, on root colonization and growth of Eucalyptus globulus and E. urophylla.Crossref | GoogleScholarGoogle Scholar |
Chen YL, Kang LH, Malajczuk N, Dell B (2006) Selecting ectomycorrhizal fungi for inoculating plantations in south China: effect of Scleroderma on colonization and growth of exotic Eucalyptus globulus, E. urophylla, Pinus elliottii, and P. radiata. Mycorrhiza 16, 251–259.
| Selecting ectomycorrhizal fungi for inoculating plantations in south China: effect of Scleroderma on colonization and growth of exotic Eucalyptus globulus, E. urophylla, Pinus elliottii, and P. radiata.Crossref | GoogleScholarGoogle Scholar | 16534620PubMed |
Chen YL, Liu S, Dell B (2007) Mycorrhizal status of Eucalyptus plantations in South China and implications for management. Mycorrhiza 17, 527–535.
| Mycorrhizal status of Eucalyptus plantations in South China and implications for management.Crossref | GoogleScholarGoogle Scholar | 17406907PubMed |
Chilvers GA (1973) Host range of some eucalypt mycorrhizal fungi. Australian Journal of Botany 21, 103–111.
| Host range of some eucalypt mycorrhizal fungi.Crossref | GoogleScholarGoogle Scholar |
Chilvers GA (2000) Mycorrhizas of eucalypts. In ‘Diseases and pathogens of eucalypts’. (Eds PJ Keane, GA Kile, FD Podger, BN Brown) pp. 71–101. (CSIRO Publishing: Melbourne)
Chu-Chou M, Grace LJ (1982) Mycorrhizal fungi of Eucalyptus in north island of New Zealand. Soil Biology & Biochemistry 14, 133–137.
| Mycorrhizal fungi of Eucalyptus in north island of New Zealand.Crossref | GoogleScholarGoogle Scholar |
Chu-Chou M, Grace LJ (1983) Hypogeous fungi associated with some forest trees in New Zealand. New Zealand Journal of Botany 21, 183–189.
| Hypogeous fungi associated with some forest trees in New Zealand.Crossref | GoogleScholarGoogle Scholar |
Dell B, Malajczuk N, Dunstan WA (2002) Persistence of some Australian Pisolithus species introduced into eucalypt plantations in china. Forest Ecology and Management 169, 271–281.
| Persistence of some Australian Pisolithus species introduced into eucalypt plantations in china.Crossref | GoogleScholarGoogle Scholar |
Ducousso M, Duponnois R, Thoen D, Prin Y (2012) Diversity of ectomycorrhizal fungi associated with Eucalyptus in Africa and Madagascar. International Journal of Forestry Research 2012, 1–10.
| Diversity of ectomycorrhizal fungi associated with Eucalyptus in Africa and Madagascar.Crossref | GoogleScholarGoogle Scholar |
Garbaye J, Delwaulle JC, Diangana D (1988) Growth response of eucalypts in the Congo to ectomycorrhizal inoculation. Forest Ecology and Management 24, 151–157.
| Growth response of eucalypts in the Congo to ectomycorrhizal inoculation.Crossref | GoogleScholarGoogle Scholar |
Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes – application to the identification of mycorrhizae and rusts. Molecular Ecology 2, 113–118.
Gardner JH, Malajczuk N (1988) Recolonisation of rehabilitated bauxite mine sites in Western Australia by mycorrhizal fungi. Forest Ecology and Management 24, 27–42.
| Recolonisation of rehabilitated bauxite mine sites in Western Australia by mycorrhizal fungi.Crossref | GoogleScholarGoogle Scholar |
Hall IR, Brown GD, Byars J (1995) ‘The black truffle – its history, uses and cultivation.’ (New Zealand Crop and Food Research: Christchurch)
Hameed A, Aleem A, Anwar AA, Anwar HG (2002) Diversity of plant species in Lal Suhanra National Park, Bahawalpur, Pakistan. The Journal of Biological Sciences 2, 267–274.
| Diversity of plant species in Lal Suhanra National Park, Bahawalpur, Pakistan.Crossref | GoogleScholarGoogle Scholar |
Hanif M, Khalid AN, Sarwar S (2012) Additions to ectomycorrhizae associated with Himalayan cedar (Cedrus deodara) using rDNA-ITS. International Journal of Agriculture and Biology 13, 1062–1067.
Horton TR, Bruns TD (2001) The molecular revolution in ectomycorrhizal ecology. Molecular Ecology 10, 1855–1871.
Jabeen S, Khalid AN (2014) Community structure of ectomycorrhizae associated with Salix spp. growing in two different climatic regions of Pakistan. International Journal of Agriculture and Biology 16, 480–488.
Jabeen S, Ilyas S, Niazi AR, Khalid AN (2012) Diversity of ectomycorrhizae associated with Populus spp., growing in two different ecological zones of Pakistan. International Journal of Agriculture and Biology 14, 681–688.
Kabre A (1982) Mycorhization de Pinus caribaea (Morelet) var. Hondurensis dans différents sols du Sénégal. Thèse de doctorat, Université Nancy I, Nancy.
Kazmi SAR, Khalid AN, Niazi AR (2004) Ectomycorrhizal diversity with Himalayan Poplar (Populus ciliata Wall ex Royle). Mycopath 2, 75–78.
Khalid AN, Niazi AR (2003) New ectomycorrhizas in association with Popular from Himalayan moist temperate forests of Pakistan. Mycopath 1, 95–98.
Khalid AN, Khurshid S, Firdaus-E-Bareen (1998) Pinirrhiza alba – a new ectomycorrhiza from Lahore. Pakistan Journal of Forestry 48, 47–54.
Khan I, Marwat KB, Khan IA, Ali H, Dawar K, Khan H (2011) Invasive weeds of southern districts of Khyber Pakhtunkhwa–Pakistan. Pakistan Journal of Weed Science Reasearch 17, 161–174.
Lampky JR, Peterson JE (1963) Pisolithus tinctorius associated with pines in Missouri. Mycologia 55, 675–678.
| Pisolithus tinctorius associated with pines in Missouri.Crossref | GoogleScholarGoogle Scholar |
Lei J, Lapeyrie F, Malajczuk N, Dexheimer J (1990) Infectivity of pine and eucalypt isolates of Pisolithus tinctorius on roots of Eucalyptus urophylla in vitro. II. Ultrastructural and biochemical changes at the early stage of mycorrhiza formation. New Phytologist 116, 115–122.
| Infectivity of pine and eucalypt isolates of Pisolithus tinctorius on roots of Eucalyptus urophylla in vitro. II. Ultrastructural and biochemical changes at the early stage of mycorrhiza formation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXpvVCrsA%3D%3D&md5=c316f113dcb6a7875c77f20ec96d9b9cCAS |
Lu XH, Malajczuk N, Dell B (1998) Mycorrhiza formation and growth of Eucalyptus globulus seedlings inoculated with spores of various ectomycorrhizal fungi. Mycorrhiza 8, 81–86.
| Mycorrhiza formation and growth of Eucalyptus globulus seedlings inoculated with spores of various ectomycorrhizal fungi.Crossref | GoogleScholarGoogle Scholar |
Lu XH, Malajczuk N, Brundrett M, Dell B (1999) Fruiting of putative ectomycorrhizal fungi under blue gum (Eucalyptus globulus) plantations of different ages in Western Australia. Mycorrhiza 8, 255–261.
| Fruiting of putative ectomycorrhizal fungi under blue gum (Eucalyptus globulus) plantations of different ages in Western Australia.Crossref | GoogleScholarGoogle Scholar |
Malajczuk M, Hingston FJ (1981) Ectomycorrhizae associated with Jarrah. Australian Journal of Botany 29, 453–462.
| Ectomycorrhizae associated with Jarrah.Crossref | GoogleScholarGoogle Scholar |
Malajczuk N, Lapeyrie F, Garbaye J (1990) Infectivity of pine and eucalypt isolates of Pisolithus tinctorius on roots of Eucalyptus urophylla in vitro. New Phytologist 114, 627–631.
| Infectivity of pine and eucalypt isolates of Pisolithus tinctorius on roots of Eucalyptus urophylla in vitro.Crossref | GoogleScholarGoogle Scholar |
Martin TP, Harris JR, Eaton GK, Miller OK (2003) The efficacy of ectomycorrhizal colonization of pine and scarlet oak in nursery production. Journal of Environmental Horticulture 21, 45–50.
Marx DH, Hedin A, Toe SFP (1985) Field performance of Pinus caribaea var. hondurensis seedlings with specific ectomycorrhizae and fertilizer after three years on a savanna site in Liberia. Forest Ecology and Management 13, 1–25.
| Field performance of Pinus caribaea var. hondurensis seedlings with specific ectomycorrhizae and fertilizer after three years on a savanna site in Liberia.Crossref | GoogleScholarGoogle Scholar |
Mason PA, Ingleby K, Munro RC, Wilson J, Ibrahim K (2000) The effect of reduced phosphorus concentration on mycorrhizal development and growth of Eucalyptus globulus Labill. seedlings inoculated with 10 different fungi. Forest Ecology and Management 128, 249–258.
| The effect of reduced phosphorus concentration on mycorrhizal development and growth of Eucalyptus globulus Labill. seedlings inoculated with 10 different fungi.Crossref | GoogleScholarGoogle Scholar |
Mikola P (1970) Mycorrhizal inoculation in afforestation. International Review of Forestry Research 3, 123–196.
| Mycorrhizal inoculation in afforestation.Crossref | GoogleScholarGoogle Scholar |
Niazi AR (2008) ‘Biodiversity of ectomycorrhizas in conifers from Himalayan Moist Temperate forests of Pakistan’. PhD thesis, Department of the Botany, University of the Punjab, Pakistan.
Niazi AR, Iqbal SH, Khalid AN (2006) Russula brevipes Peck. its ectomycorrhiza, a new record from Himalayan Moist Temperate Forests of Pakistan. Pakistan Journal of Botany 38, 1271–1277.
Niazi AR, Khalid AN, Iqbal SH (2007) Descolea flavoannulata and its ectomycorrhiza from Pakistan’s Himalayan moist temperate forests. Mycopath 101, 375–383.
Niazi AR, Iqbal SH, Khalid AN (2009) Ectomycorrhizae between Amanita rubescens Himalayan Spruce (Picea smithiana) from Pakistan. Mycotaxon 107, 73–80.
| Ectomycorrhizae between Amanita rubescens Himalayan Spruce (Picea smithiana) from Pakistan.Crossref | GoogleScholarGoogle Scholar |
Niazi AR, Khalid AN, Iqbal SH (2010) New records of ectomycorrhizae from Pakistan. Pakistan Journal of Botany 24, 4335–4343.
Pampolina NM, De la Cruz RE, Garcia MU (2002) Dynamics of ectomycorrhizal fungi in an Eucalyptus globulus plantation: effect of phosphorus fertilization. Forest Ecology and Management 158, 291–304.
| Dynamics of ectomycorrhizal fungi in an Eucalyptus globulus plantation: effect of phosphorus fertilization.Crossref | GoogleScholarGoogle Scholar |
Razzaq A, Shahzad S (2004) Pisolithus tinctorius, a new record from Pakistan. Pakistan Journal of Botany 36, 449–451.
Sarwar S, Hanif M, Khalid AN, Guinberteau J (2011) Diversity of Boletes in Pakistan; focus on Suillus brevipes and Suillus sibiricus. In ‘Proceedings of the 7th international conference on mushroom biology and mushroom products, Arcachon, France’. Vol. 1, pp. 123–133. Available at http://prodinra.inra.fr/ft?id=ABC4AB39-8E12-47C6-A53F-52B97B6ACBB9
Sarwar S, Khalid AN, Hanif M, Niazi AR (2012) Suillus falvidus and its ectomycorrhizae with Pinus walichiana in Pakistan. Mycotaxon 12, 225–232.
Sarwar S, Jabeen S, Khalid AN (2013) Additions to ectomycorrhizae associated with Populus ciliata Wall. Ex Royle from Pakistan. Journal of Yeast and Fungal Reasearch 4, 98–102.
Thapar HS, Singh B, Bakshi BK (1967) Mycorrhizae in Eucalyptus. Indian Forester 93, 756–759.
Thoen D, Ducousso M (1990) Mycorrhizal habit and sclerogenesis of Phlepobus sudanicus (Gyrodontaceae) in Senegal. Agriculture, Ecosystems & Environment 28, 519–523.
| Mycorrhizal habit and sclerogenesis of Phlepobus sudanicus (Gyrodontaceae) in Senegal.Crossref | GoogleScholarGoogle Scholar |
Thomson BD, Hardy GJ, Malajczuk N, Grove TS (1996) The survival and development of inoculant ectomycorrhizal fungi on roots of outplanted Eucalyptus globulus Labill. Plant and Soil 178, 247–253.
| The survival and development of inoculant ectomycorrhizal fungi on roots of outplanted Eucalyptus globulus Labill.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XitVahsLs%3D&md5=7e1331ea6ee30d38a7177445f2fdc120CAS |
