New insights into the polyploid complex Cenchrus ciliaris L. (Poaceae) show its capacity for gene flow and recombination processes despite its apomictic nature
Amina Kharrat-Souissi A E , Alex Baumel B , Franck Torre B , Marianick Juin B , Sonja Siljak-Yakovlev C , Anne Roig D and Mohamed Chaieb AA Faculté des Sciences, Département de Biologie, Laboratoire de Biologie et d’Ecophysiologie des végétaux en milieu aride, Université de Sfax, Tunisie.
B Institut Méditerranéen d’Ecologie et de Paléoécologie, UMR-CNRS/IRD 6116 IMEP – Bâtiment Villemin, Europole de l’Arbois – BP 80, 13545 Aix-en-Provence Cedex 04, France.
C Université Paris-Sud UMR 8079, Département de Biodiversité Systématique & Évolution, Bâtiment 36091405 Orsay Cedex, France.
D Centre INRA PACA, Domaine de Saint Paul URFM, Unité Écologie des Forêts Méditerranéennes, 84914 Avignon, France.
E Corresponding author. Email: kharratsouissi@yahoo.fr
Australian Journal of Botany 59(6) 543-553 https://doi.org/10.1071/BT10312
Submitted: 24 November 2010 Accepted: 29 August 2011 Published: 5 October 2011
Abstract
Cenchrus ciliaris L. is a C4 perennial grass of arid lands which is under the focus of different ecological issues such as response to desertification, quality of forage grass and impacts of invasions. Here, molecular and morphological analyses of the genetic diversity of several Tunisian provenances of C. ciliaris were performed to better understand the phenotypic polymorphism of this agamospermous and polyploid grass. Ten phenotypic traits associated with productivity were measured in a common garden environment. Amplified Fragment Length Polymorphism (AFLP) markers were developed to investigate the structure of genetic diversity among and within provenances and between the three ploidy levels. Heritable phenotypic traits showed considerable differences within provenances. Surprisingly, AFLP markers revealed the existence of genotypic variations between individuals of the same sibship and a high G/N value (0.55). A neighbour-joining tree based on AFLP markers revealed three major groups; tetraploid, pentaploid and a mix of pentaploid and hexaploids. These groups do not correspond completely to the geographical origin of samples. The results underline the possibility of sexual reproduction, recombination and gene flow within and between populations of C. ciliaris. In respect with the well known dynamic nature of polyploid genomes, these results should have strong consequences for the future management of this grass for both conservation and invasion issues.
References
Ainouche ML, Jenczewski E (2010) Focus on polyploidy. New Phytologist 186, 1–4.| Focus on polyploidy.Crossref | GoogleScholarGoogle Scholar |
Ainouche ML, Fortune P, Salmon A, Parisod C, Grandbastien MA, Fukunaga K, Ricou M, Misset MT (2009) Hybridization, polyploidy and invasion: lessons from Spartina (Poaceae). Biological Invasions 11, 1159–1173.
| Hybridization, polyploidy and invasion: lessons from Spartina (Poaceae).Crossref | GoogleScholarGoogle Scholar |
Al-Soqeer A (2011) Genotypic diversity among wild populations of Buffelgrass (Cenchrus ciliaris L. Link) in Al-Qassim region. Asian Journal of Biotechnology 3, 262–268.
| Genotypic diversity among wild populations of Buffelgrass (Cenchrus ciliaris L. Link) in Al-Qassim region.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXovVKjsbs%3D&md5=cef9379cada9df4fa3491065c6158a60CAS |
Arshad M, Ashraf MY, Ahmad M, Zaman F (2007) Morpho-genetic variability potential of Cenchrus ciliaris L. from Cholistan desert, Pakistan. Pakistan Journal of Botany 39, 1481–1488.
Arshadullah M, Malik MA, Rasheed M, Jilani G, Zahoor F, Kaleem S (2011) Seasonal and genotypic variations influence the biomass and nutritional ingredients of Cenchrus ciliaris grass forage. International Journal Agriculture and Biology 13, 120–124.
Bashaw EC, Hignight KW (1990) Gene transfer in apomictic Buffelgrass through fertilization of an unreduced egg. Crop Science 30, 571–575.
| Gene transfer in apomictic Buffelgrass through fertilization of an unreduced egg.Crossref | GoogleScholarGoogle Scholar |
Baumel A, Ainouche ML, Levasseur JE (2001) Molecular investigations in populations of Spartina anglica C.E. Hubbard (Poaceae) invading coastal Brittany (France). Molecular Ecology 10, 1689–1701.
| Molecular investigations in populations of Spartina anglica C.E. Hubbard (Poaceae) invading coastal Brittany (France).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlvVyns7w%3D&md5=d92e0c09e8f486f6594137b3dc82617fCAS |
Bayer RJ (1983) Distribution of sexual and apomict populations of Antennaria parlinii. Evolution 37, 555–561.
| Distribution of sexual and apomict populations of Antennaria parlinii.Crossref | GoogleScholarGoogle Scholar |
Bayer RJ (1990) Patterns of clonal diversity in the Antennaria rosea (Asteraceae) polyploid agamic complex. American Journal of Botany 77, 1313–1319.
| Patterns of clonal diversity in the Antennaria rosea (Asteraceae) polyploid agamic complex.Crossref | GoogleScholarGoogle Scholar |
Bousquet B (Ed.) (1992) ‘Guide des parcs nationaux d’Afrique (Afrique du Nord, de l’Ouest).’ (Delachaux et Niestlé: Paris, France)
Bray RR (1978) Evidence for facultative apomixis in Cenchrus ciliaris. Euphytica 27, 801–804.
| Evidence for facultative apomixis in Cenchrus ciliaris.Crossref | GoogleScholarGoogle Scholar |
Brits G, Trysman M, Smith A, Ndlovu S, Mogale E, Makhafula M, Molifi R (2003) Screenings of subtropical grass species for drought tolerance. In ‘Proceedings of the VIIth International Rangelands Congress’ (Eds. N Allsopp, AR Palmer, SJ Milton, KP Kirkman, GIH Kerley, CR Hurt, CJ Brown). Produced by Document Transformation Technologies. pp. 1348–1350. (Durban, South Africa)
Carino DA, Daehler CC (1999) Genetic variation in an apomictic grass, Heteropogon contortus, in the Hawaiian Islands. Molecular Ecology 8, 2127–2132.
| Genetic variation in an apomictic grass, Heteropogon contortus, in the Hawaiian Islands.Crossref | GoogleScholarGoogle Scholar |
Chaieb M, Floret C, Le Floc’h E, Pontanier R (1992) Life history strategies and water resources allocation in five pasture species of the Tunisian arid zone. Arid Soil Research and Rehabilitation 6, 1–10.
Chapman HM, Parh D, Oraguzie N (2000) Genetic structure and colonizing success of a clonal, weedy species, Pilosella officinarum (Asteraceae). Heredity 84, 401–409.
| Genetic structure and colonizing success of a clonal, weedy species, Pilosella officinarum (Asteraceae).Crossref | GoogleScholarGoogle Scholar |
Chapman MA, Abbott RJ (2010) Introgression of fitness genes across a ploidy barrier. New Phytologist 186, 63–71.
| Introgression of fitness genes across a ploidy barrier.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXkvVOktrs%3D&md5=8f704249713495e4feeff35c98eb67b6CAS |
Cosendai AC, Hörandl E (2010) Cytotype stability, facultative apomixis and geographical parthenogenesis in Ranunculus kuepferi (Ranunculaceae). Annals of Botany 105, 457–470.
| Cytotype stability, facultative apomixis and geographical parthenogenesis in Ranunculus kuepferi (Ranunculaceae).Crossref | GoogleScholarGoogle Scholar |
Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin 19, 11–15.
Duke JA (1983) Cenchrus ciliaris L. Handbook of energy crops. Available at http://www.hort.purdue.edu/newcrop/duke_energy/Cenchrus_ciliaris.html [Verified 1 September 2011]
Emberger A (1945) Une classification biogéographique des climats. Recueil des travaux des laboratoires de botanique, de géologie et zoologie de la Faculté des Sciences de l’Université de Montpellier. Série Botanique 7, 3–43.
Fisher WD, Bashaw EC, Holt EC (1954) Evidence for apomixis in Pennisetum ciliare and Cenchrus setigerus. Agronomy Journal 46, 401–404.
| Evidence for apomixis in Pennisetum ciliare and Cenchrus setigerus.Crossref | GoogleScholarGoogle Scholar |
Grant V (1971) ‘Plant speciation.’ (Colombia University Press: New York)
Gutierrez-Ozuna R, Eguiarte LE, Molina-Freaner F (2009) Genotypic diversity among pasture and roadside populations of the invasive buffelgrass (Pennisetum ciliare L. Link) in north-western Mexico. Journal of Arid Environments 73, 26–32.
| Genotypic diversity among pasture and roadside populations of the invasive buffelgrass (Pennisetum ciliare L. Link) in north-western Mexico.Crossref | GoogleScholarGoogle Scholar |
Heslop-Harrison J (1961) Apomixis, environment and adaptation. In ‘Recent advances in botany’. (Ed. DL Bailey) pp. 891–895. (University Toronto Press: Toronto)
Hignight KW, Bashaw EC, Hussey MA (1991) Cytological and morphological diversity of native apomictic buffelgrass. Botanical Gazette (Chicago, Ill.) 152, 214–218.
| Cytological and morphological diversity of native apomictic buffelgrass.Crossref | GoogleScholarGoogle Scholar |
Jackson J (2004) Impacts and management of Cenchrus ciliaris (Buffel Grass) as an invasive species in northern Queesland. Thesis in tropical plant sciences, James Cook University of North Queesland. Australia
Jauffret S, Lavorel S (2003) Are plant functional types relevant to describe degradation in arid, southern Tunisian steppes? Journal of Vegetation Science 14, 399–408.
| Are plant functional types relevant to describe degradation in arid, southern Tunisian steppes?Crossref | GoogleScholarGoogle Scholar |
Kassas M (1995) Desertification: a general review. Journal of Arid Environments 30, 115–128.
| Desertification: a general review.Crossref | GoogleScholarGoogle Scholar |
Kharrat-Souissi A, Baumel A, Mseddi K, Torre F, Chaieb M (2010) Polymorphism of Cenchrus ciliaris L. a perennial grass of arid zones. African Journal of Ecology 49, 209–220.
| Polymorphism of Cenchrus ciliaris L. a perennial grass of arid zones.Crossref | GoogleScholarGoogle Scholar |
Lavergne S, Molofsky J (2007) Increased genetic variation and evolutionary potential drive the success of an invasive grass. Proceedings of the National Academy of Sciences of the United States of America 104, 3883–3888.
| Increased genetic variation and evolutionary potential drive the success of an invasive grass.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjtlaisbo%3D&md5=6e96081907eae1de018457a2e416c163CAS |
Le Roux JJ, Wieczorek AM, Wright MG, Tran CT (2007) Super-Genotype: global monoclonality defies the odds of nature. PLoS ONE 2, e590
| Super-Genotype: global monoclonality defies the odds of nature.Crossref | GoogleScholarGoogle Scholar |
Li C, Hao X, Zhao M, Han G, Willms WD (2008) Influence of historic sheep grazing on vegetation and soil properties of a Desert Steppe in Inner Mongolia. Agriculture Ecosystems & Environment 128, 109–116.
| Influence of historic sheep grazing on vegetation and soil properties of a Desert Steppe in Inner Mongolia.Crossref | GoogleScholarGoogle Scholar |
Mansoor U, Hameed M, Wahid A, Rao AR (2002) Ecotypic variability for drought resistance in Cenchrus ciliaris L. germplasm from Cholistan Desert in Pakistan. International Jouranl of Agriculture and Biology 4, 392–397.
Migliore J, Baumel A, Juin M, Diadema K, Hugot L, Verlaque R, Médail F (2011) Genetic diversity and structure of a Mediterranean endemic plant in Corsica (Mercurialis corsica, Euphorbiaceae). Population Ecology 53, 573–586.
| Genetic diversity and structure of a Mediterranean endemic plant in Corsica (Mercurialis corsica, Euphorbiaceae).Crossref | GoogleScholarGoogle Scholar |
Miller TK, Allen CR, Landis WG, Merchant JW (2010) Risk assessment: simultaneously prioritizing the control of invasive plant species and the conservation of rare plant species. Biological Conservation 143, 2070–2079.
| Risk assessment: simultaneously prioritizing the control of invasive plant species and the conservation of rare plant species.Crossref | GoogleScholarGoogle Scholar |
Mnif L, Mseddi K, Chaieb M, Roux M (2003) Diversité génétique chez diverses provenances de Cenchrus ciliaris L. graminée prenne de la zone aride tunisienne. Bocconea 16, 641–656.
M’Seddi K (2005) Analyse comparative des caractéristiques biologiques de différentes provenances de Cenchrus ciliaris L., une graminée pérenne de la zone aride tunisienne. Thèse de Doctorat, Faculté des Sciences de Sfax, Tunisie.
M’Seddi K, Visser M, Neffati M, Reheul D, Chaieb M (2002) Seed and spike traits from remnant populations of Cenchrus ciliaris L., in South Tunisia: high distinctiveness, no ecotypes. Journal of Arid Environments 50, 309–324.
| Seed and spike traits from remnant populations of Cenchrus ciliaris L., in South Tunisia: high distinctiveness, no ecotypes.Crossref | GoogleScholarGoogle Scholar |
M’Seddi K, Mnif L, Neffati M, Chaieb M, Roux M (2004) Aboveground phytomass productivity and morphological variability of Tunisian accessions of Cenchrus ciliaris L. African Journal of Range and Forage Science 21, 49–55.
| Aboveground phytomass productivity and morphological variability of Tunisian accessions of Cenchrus ciliaris L.Crossref | GoogleScholarGoogle Scholar |
Novak SJ, Mack RN (2000) Clonal diversity within and among introduced populations of the apomictic vine Bryonia alba (Cucurbitaceae). Canadian Journal of Botany 78, 1469–1481.
Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annual Review of Ecology and Systematics 37, 637–669.
| Ecological and evolutionary responses to recent climate change.Crossref | GoogleScholarGoogle Scholar |
Peakall R, Smouse PE (2006) GenAlEx 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6, 288–295.
| GenAlEx 6: genetic analysis in Excel. Population genetic software for teaching and research.Crossref | GoogleScholarGoogle Scholar |
Poulin J, Weller SG, Sakai AK (2005) Genetic diversity does not affect the invasiveness of fountain grass (Pennisetum setaceum) in Arizona, California and Hawaii. Diversity & Distributions 11, 241–247.
| Genetic diversity does not affect the invasiveness of fountain grass (Pennisetum setaceum) in Arizona, California and Hawaii.Crossref | GoogleScholarGoogle Scholar |
R Development Core Team (2009) ‘R: language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna, Austria) Available at http://www.R-project.org [Verified 1 September 2011]
Reynolds JF, Stafford Smith DM, Lambin EF, Turner II BL, Mortimore M, Batterbury SPJ, Downing TE, Dowlatabadi H, Fernández RJ, Herrick JE, Huber-Sannvald E, Leemans R, Lynam T, Maestre FT, Ayarza M, Walker B (2007) Global desertification: building a science for dryland development. Science 316, 847–851.
| Global desertification: building a science for dryland development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXltVentb4%3D&md5=948fc81b73e0873e35ff234b8b3722abCAS |
Sherwood RT, Young BA, Bashaw EC (1980) Facultative apomixis in buffelgrass. Crop Science 20, 375–379.
| Facultative apomixis in buffelgrass.Crossref | GoogleScholarGoogle Scholar |
Snyder LA, Alice RH, Warmke HE (1955) The mechanisms of apomixis in Pennisetum ciliare. Botanical Gazette (Chicago, Ill.) 116, 209–221.
| The mechanisms of apomixis in Pennisetum ciliare.Crossref | GoogleScholarGoogle Scholar |
Thioulouse J, Chessel D, Dolédec S, Olivier JM (1997) ADE-4: A multivariate analysis and graphical display software. Statistics and Computing 7, 75–83.
Valone TJ, Meyer M, Brown JH, Chew RM (2002) Timescale of perennial grass recovery in desertified grasslands following livestock removal. Conservation Biology 16, 995–1002.
| Timescale of perennial grass recovery in desertified grasslands following livestock removal.Crossref | GoogleScholarGoogle Scholar |
Van Der Hulst RG, Mes TH, Den Nijs JC, Bachmann K (2000) Amplified fragment length polymorphism (AFLP) markers reveal that population structure of triploid dandelions (Taraxacum officinale) exhibits both clonality and recombination. Molecular Ecology 9, 1–8.
| Amplified fragment length polymorphism (AFLP) markers reveal that population structure of triploid dandelions (Taraxacum officinale) exhibits both clonality and recombination.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c7hslGrsA%3D%3D&md5=178261e941ae44a2596d326e361380e7CAS |
Vekemans X, Beauwens T, Lemaire M, Roldán-Ruiz I (2002) Data from amplified fragment length polymorphism (AFLP) markers show indication of size homoplasy and of a relationship between degree of homoplasy and fragment size. Molecular Ecology 11, 139–151.
| Data from amplified fragment length polymorphism (AFLP) markers show indication of size homoplasy and of a relationship between degree of homoplasy and fragment size.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD387ntVSquw%3D%3D&md5=3d10d810611fece6a0b9508177ae135dCAS |
Visser M, Mseddi K, Chaïeb M, Neffati M (2008) Assessing yield and yield stability of remnant populations of Cenchrus ciliaris L. in arid Tunisia: developing a blueprint for initiating native seed production. Grass and Forage Science 63, 301–313.
| Assessing yield and yield stability of remnant populations of Cenchrus ciliaris L. in arid Tunisia: developing a blueprint for initiating native seed production.Crossref | GoogleScholarGoogle Scholar |
Vos P, Hogers R, Bleeker M, Reijans M, Lee TV, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M, Zabeau M (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Research 23, 4407–4414.
| AFLP: a new technique for DNA fingerprinting.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXpslensbo%3D&md5=62efaf0c7670de02b9d606e4e15ade28CAS |
Whitford WG (2002) ‘Ecology of desert systems.’ (Academic Press: London)
Yannic G, Baumel A, Ainouche M (2004) Uniformity of the nuclear and chloroplast genomes of Spartina maritima (Poaceae), a salt-marsh species in decline along the Western European Coast. Heredity 93, 182–188.
| Uniformity of the nuclear and chloroplast genomes of Spartina maritima (Poaceae), a salt-marsh species in decline along the Western European Coast.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlvFCqsb0%3D&md5=33bc3e8e584eabb8041d2d3953bc0879CAS |
Yates CJ, Norton DA, Hobbs RJ (2000) Grazing effects on plant cover, soil and microclimate in fragmented woodlands in south-western Australia: implications for restoration. Austral Ecology 25, 36–47.
| Grazing effects on plant cover, soil and microclimate in fragmented woodlands in south-western Australia: implications for restoration.Crossref | GoogleScholarGoogle Scholar |