Hostname: page-component-848d4c4894-4hhp2 Total loading time: 0 Render date: 2024-05-06T10:55:37.944Z Has data issue: false hasContentIssue false

Diversity in the trifoliate orange taxon reveals two main genetic groups marked by specific morphological traits and water deficit tolerance properties

Published online by Cambridge University Press:  24 March 2015

J. BEN YAHMED
Affiliation:
CIRAD, UMR AGAP, TA A-108/02, 34398 Montpellier, Cedex 5, France
G. COSTANTINO
Affiliation:
INRA, UMR AGAP Corse, 20230 San Giuliano, France
P. AMIEL
Affiliation:
CIRAD, UMR AGAP, TA A-108/02, 34398 Montpellier, Cedex 5, France
M. TALON
Affiliation:
IVIA; Centro de Genomica, Ctra. Moncada-Náquera Km 5, 46113 Moncada, Valencia, Spain
P. OLLITRAULT
Affiliation:
CIRAD, UMR AGAP, TA A-108/02, 34398 Montpellier, Cedex 5, France
R. MORILLON
Affiliation:
CIRAD, UMR AGAP, TA A-108/02, 34398 Montpellier, Cedex 5, France IVIA; Centro de Genomica, Ctra. Moncada-Náquera Km 5, 46113 Moncada, Valencia, Spain
F. LURO*
Affiliation:
INRA, UMR AGAP Corse, 20230 San Giuliano, France
*
*To whom all correspondence should be addressed. Email: luro@corse.inra.fr

Summary

Trifoliate orange (Poncirus trifoliata (L.) Raf.) is a very useful taxon for the citrus industry since this rootstock is immune to the Citrus Tristeza virus and confers cold tolerance. Numerous trifoliate orange varieties exist but little is known regarding their behavioural variability when subjected to abiotic constraints. The diversity of 74 P. trifoliata accessions maintained in the INRA-CIRAD Citrus Germplasm Collection was investigated using simple sequence repeat markers. Two major genetic groups were clearly identified as a few homonyms, intergroup or intra-group hybrids and doubled-chromosome tetraploid forms. The Group 1 phenotype was characterized by larger flowers and leaves and smaller seeds than Group 2. Tetraploid accessions showed larger leaves and heavier seeds than all other diploid accessions, regardless of genetic classification. Eight genotypes belonging to both genetic groups, as well as two hybrids between the two groups, were selected to investigate their water deficit tolerance. Stress was applied by withdrawing irrigation for 4 weeks. Physiological parameters such as leaf stomatal conductance, quantum yield of photosystem II electron transport, soil water potential, leaf osmotic potential and transpiration rate were estimated. Some varieties, such as Rubidoux 0101033, were clearly more tolerant to water deficit than others, such as Pomeroy 0101040 and Pomeroy 0110081. Interestingly, accessions that had the highest soil water potential and were the least affected by stress belonged to genetic Group 2. Conversely, trifoliate oranges of genetic Group 1 were the least tolerant.

Type
Crops and Soils Research Papers
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Aka Kaçar, Y., Yeşİloğlu, T., Yildirim, B., Sİmşek, O., Incesu, M., Kamİloğlu, M. & Tuzcu, O. (2009). Genetic characterization of some citrus rootstock by using SSR markers. Alatarim 8, 816.Google Scholar
Aleza, P., Froelicher, Y., Schwarz, S., Agusti, M., Hernandez, M., Juarez, J., Luro, F., Morillon, R., Navarro, L. & Ollitrault, P. (2011). Tetraploidization events by chromosome doubling of nucellar cells are frequent in apomictic citrus and are dependent on genotype and environment. Annals of Botany 108, 3750.CrossRefGoogle ScholarPubMed
Allario, T., Brumos, J., Colmenero-Flores, J. M., Tadeo, F., Froelicher, Y., Talon, M., Navarro, L., Ollitrault, P. & Morillon, R. (2011). Large changes in anatomy and physiology between diploid Rangpur lime (Citrus limonia) and its autotetraploid are not associated with large changes in leaf gene expression. Journal of Experimental Botany 62, 25072519.Google Scholar
Anderson, C. M., Castle, W. S. & Moore, G. A. (1991). Isozymic identification of zygotic seedlings in Swingle citrumelo Citrus paradisi × Poncirus trifoliata nursery and field populations. Journal of the American Society for Horticultural Science 116, 322326.CrossRefGoogle Scholar
Arbona, V., Manzi, M., Ollas, C. d. & Gómez-Cadenas, A. (2013). Metabolomics as a tool to investigate abiotic stress tolerance in plants. International Journal of Molecular Sciences 14, 48854911.CrossRefGoogle ScholarPubMed
Ashraf, M. & Foolad, M. R. (2007). Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environmental and Experimental Botany 59, 206216.Google Scholar
Balal, R. M., Khan, M. M., Shahid, M. A., Mattson, N. S., Abbas, T., Ashfaq, M., Garcia-Sanchez, F., Ghazanfer, U., Gimeno, V. & Iqbal, Z. (2012). Comparative studies on the physiobiochemical, enzymatic, and ionic modifications in salt-tolerant and salt-sensitive Citrus rootstocks under NaCl stress. Journal of the American Society for Horticultural Science 137, 8695.Google Scholar
Bates, L. S., Waldren, R. P. & Teare, I. D. (1973). Rapid determination of free proline for water-stress studies. Plant and Soil 39, 205207.CrossRefGoogle Scholar
Boava, L. P., Cristofani-Yaly, M., Mafra, V. S., Kubo, K., Kishi, L. T., Takita, M. A., Ribeiro-Alves, M. & Machado, M. A. (2011). Global gene expression of Poncirus trifoliata, Citrus sunki and their hybrids under infection of Phytophthora parasitica . BMC Genomics 12, 39. doi:10.1186/1471-2164-12-39.Google Scholar
Cabasson, C. M., Luro, F., Ollitrault, P. & Grosser, J. W. (2001). Non-random inheritance of mitochondrial genomes in Citrus hybrids produced by protoplast fusion. Plant Cell Reports 20, 604609.Google Scholar
Callister, A. N., Arndt, S. K. & Adams, M. A. (2006). Comparison of four methods for measuring osmotic potential of tree leaves. Physiologia Plantarum 127, 383392.CrossRefGoogle Scholar
Cantuarias-Avilés, T., Mourão-Filho, F. A. A., Stuchi, E. S., da Silva, S. R. & Espinoza-Núñez, E. (2010). Tree performance and fruit yield and quality of ‘Okitsu'Satsuma mandarin grafted on 12 rootstocks. Scientia Horticulturae 123, 318322.Google Scholar
Castle, W. S. (1987). Citrus rootstocks. In Rootstocks for Fruit Crops (Eds Rom, R. C. & Carlson, R. F.), pp. 361399. New York: Wiley.Google Scholar
Chalhoub, B. A., Thibault, S., Laucou, V., Rameau, C., Höfte, H. & Cousin, R. (1997). Silver staining and recovery of AFLP amplification products on large denaturing polyacrylamide gels. Biotechniques 22, 216218.Google Scholar
Chaves, M. M., Flexas, J. & Pinheiro, C. (2009). Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Annals of Botany 103, 551560.Google Scholar
Chen, Z., Cuin, T. A., Zhou, M., Twomey, A., Naidu, B. P. & Shabala, S. (2007). Compatible solute accumulation and stress-mitigating effects in barley genotypes contrasting in their salt tolerance. Journal of Experimental Botany 58, 42454255.Google Scholar
Cuenca, J., Froelicher, Y., Aleza, P., Juárez, J., Navarro, L. & Ollitrault, P. (2011). Multilocus half-tetrad analysis and centromere mapping in citrus: evidence of SDR mechanism for 2n megagametophyte production and partial chiasma interference in mandarin cv ‘Fortune’. Heredity 107, 462470.Google Scholar
Dice, L. R. (1945). Measures of the amount of ecologic association between species. Ecology 26, 297302.Google Scholar
Doyle, J. J. & Doyle, J. L. (1987). A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin 19, 1115.Google Scholar
Espinoza-Núñez, E., Mourão Filho, F. A. A., Stuchi, E. S., Cantuarias-Avilés, T. & dos Santos Dias, C. T. (2011). Performance of ‘Tahiti'lime on twelve rootstocks under irrigated and non-irrigated conditions. Scientia Horticulturae 129, 227231.Google Scholar
Fang, D. Q., Roose, M. L., Krueger, R. R. & Federici, C. T. (1997). Fingerprinting trifoliate orange germ plasm accessions with isozymes, RFLPs, and inter-simple sequence repeat markers. Theoretical and Applied Genetics 95, 211219.Google Scholar
Franks, P. J. & Beerling, D. J. (2009). Maximum leaf conductance driven by CO2 effects on stomatal size and density over geologic time. Proceedings of the National Academy of Sciences of the United States of America 106, 1034310347.CrossRefGoogle ScholarPubMed
Froelicher, Y., Dambier, D., Bassene, J. B., Costantino, G., Lotfy, S., Didout, C., Beaumont, V., Brottier, P., Risterucci, A. M., Luro, F. & Ollitrault, P. (2008). Characterization of microsatellite markers in mandarin orange (Citrus reticulata Blanco). Molecular Ecology Resources 8, 119122.Google Scholar
Garnsey, S. M., Barrett, H. C. & Hutchison, D. J. (1987). Identification of citrus tristeza virus resistance in citrus relatives and its potential applications. Phytophylactica 19, 187191.Google Scholar
Hardy, S. (2004). Growing Lemons in Australia – a Production Manual. New South Wales, Australia: NSW Department of Primary Industries.Google Scholar
Hussain, S., Curk, F., Ollitrault, P., Morillon, R. & Luro, F. (2011). Facultative apomixis and chromosome doubling are sources of heterogeneity in citrus rootstock trials: impact on clementine production and breeding selection. Scientia Horticulturae 130, 815819.Google Scholar
Jacquemond, C. & Blondel, L. (1986 a). Contribution à l’étude des porte-greffe des agrumes: le Poncirus trifoliata. Part I: Étude des caractères botaniques. Fruits 41, 303339.Google Scholar
Jacquemond, C. & Blondel, L. (1986 b). Contribution à l’étude des porte-greffe des agrumes: le Poncirus trifoliata. Part II: Étude des caractères biologiques. Fruits 41, 381392.Google Scholar
Jacquemond, C. & Blondel, L. (1986 c). Contribution à l’étude des porte-greffe des agrumes: le Poncirus trifoliata. Part III: Étude du comportement des Poncirus trifoliata après greffage. Fruits 41, 449464.Google Scholar
Jacquemond, C. & de Rocca Serra, D. (1994). Citrus rootstocks selection in Corsica for 25 years. In Proceedings of the International Society of Citriculture: Volume 1 Taxonomy, Breeding and Varieties, Rootstocks and Propagation, Plant Physiology and Ecology: 7th International Citrus Congress, Acireale, Italy, 8–13 March, 1992 (Eds Tribulato, E., Gentile, A. & Reforgiato, G.), pp. 246251. Acireale, Italy: International Society of Citriculture.Google Scholar
Jacquemond, C., Tison, G., Agostini, D., Navari, C., Roesch, M. & Vittori, D. (2004). C32 and C35 citranges: possible alternatives of rootstocks for clementine in Corsica. In Proceedings of the 10th Congress of International Society of Citriculture, Agadir, Morocco (Eds Ait-Oubahou, A. & El-Otmani, M.), pp. 321322. Agadir, Morocco: International Society of Citriculture.Google Scholar
Kepiro, I. L. & Roose, M. L. (2007). Nucellar embryony. In Citrus Genetics, Breeding and Biotechnology (Ed. Khan, I. A.), pp. 141149. London: CABI Publishing.Google Scholar
Khan, I. L. & Roose, M. L. (1988). Frequency and characteristics of nucellar and zygotic seedlings in three cultivars of trifoliate orange. Journal of the American Society for Horticultural Science 113, 105110.Google Scholar
Krueger, R. R. & Navarro, L. (2007). Citrus germplasm resources. In Citrus Genetics, Breeding and Biotechnology (Ed. Khan, I.), pp. 45140. London: CABI Publishing.CrossRefGoogle Scholar
Luro, F. L., Costantino, G., Terol, J., Argout, X., Allario, T., Wincker, P., Talon, M., Ollitrault, P. & Morillon, R. (2008). Transferability of the EST-SSRs developed on Nules clementine (Citrus clementina Hort ex Tan) to other Citrus species and their effectiveness for genetic mapping. BMC Genomics 9, 287. doi:10.1186/1471-2164-9-287.Google Scholar
Masinde, P. W., Stutzel, H., Agong, S. G. & Fricke, A. (2006). Plant growth, water relations and transpiration of two species of African nightshade (Solanum villosum Mill. ssp. miniatum (Bernh. ex Willd.) Edmonds and S. sarrachoides Sendtn.) under water-limited conditions. Scientia Horticulturae 110, 715.Google Scholar
Molinari, H. B. C., Marur, C. J., Filho, J. C. B., Kobayashi, A. K., Pileggi, M., Júnior, R. P. L., Pereira, L. F. P. & Vieira, L. G. E. (2004). Osmotic adjustment in transgenic citrus rootstock Carrizo citrange (Citrus sinensis Osb. × Poncirus trifoliata L. Raf.) overproducing proline. Plant Science 167, 13751381.Google Scholar
Moore, G. A. & Castle, W. S. (1988). Morphological and isozymic analysis of open-pollinated citrus rootstock populations. Journal of Heredity 79, 5963.Google Scholar
Morillon, R. & Chrispeels, M. J. (2001). The role of ABA and the transpiration stream in the regulation of the osmotic water permeability of leaf cells. Proceedings of the National Academy of Sciences of the United States of America 98, 1413814143.CrossRefGoogle ScholarPubMed
Novelli, V. M., Machado, M. A. & Lopes, C. R. (2000). Isoenzymatic polymorphism in Citrus spp. and Poncirus trifoliata (L.) Raf.(Rutaceae). Genetics and Molecular Biology 23, 163168.CrossRefGoogle Scholar
Nye, P. H. & Tinker, P. B. (1977). Solute Movement in the Soil–Root–System. Studies in Ecology Vol. 4. Berkeley, CA: University of California Press.Google Scholar
Ollitrault, P. & Navarro, L. (2012). Citrus. In Fruit Breeding (Eds Badenes, M. & Byrne, D.), pp. 623662. New York: Springer.Google Scholar
Ollitrault, P., Terol, J., Chen, C., Federici, C. T., Lotfy, S., Hippolyte, I., Ollitrault, F., Bérard, A., Chauveau, A., Cuenca, J., Costantino, G., Kacar, Y., Mu, L., Garcia-Lor, A., Froelicher, Y., Aleza, P., Boland, A., Billot, C., Navarro, L., Luro, F., Roose, M. L., Gmitter, F. G., Talon, M. & Brunel, D. (2012). A reference genetic map of C. clementina hort. ex Tan.; citrus evolution inferences from comparative mapping. BMC Genomics 13, 593. doi:10.1186/1471-2164-13-593.Google Scholar
Pang, X. M., Hu, C. G. & Deng, X. X. (2007). Phylogenetic relationships within Citrus and its related genera as inferred from AFLP markers. Genetic Resources and Crop Evolution 54, 429436.Google Scholar
Percival, G. C. (2005). The use of chlorophyll fluorescence to identify chemical and environmental stress in leaf tissue of three oak (Quercus) species. Journal of Arboriculture 31, 215227.Google Scholar
Perrier, X., Flori, A. & Bonnot, F. (2003). Methods of data analysis. In Genetic Diversity of Cultivated Tropical Plants (Eds Hamon, P., Seguin, M., Perrier, X. & Glaszmann, J. C.), pp. 3163. Montpellier: Science Publishers.Google Scholar
Ribeiro, R. V., Espinoza-Núñez, E., Junior, J. P., Filho, F. A. A. M. & Machado, E. C. (2014). Citrus rootstocks for improving the horticultural performance and physiological responses under constraining environments. In Improvement of Crops in the Era of Climatic Changes (Eds Ahmad, P., Wani, M. R., Azooz, M. M. & Tran, L.-S. P.), pp. 137. New York: Springer.Google Scholar
Rodríguez-Gamir, J., Primo-Millo, E., Forner, J. B. & Forner-Giner, M. A. (2010). Citrus rootstock responses to water stress. Scientia Horticulturae 126, 95102.Google Scholar
Roose, M. L. & Kupper, R. S. (1992). Causes and consequences of variability in rootstocks. In Proceeding of the First International Seminar on Citriculture in Pakistan (Ed. Khan, I. A.), pp. 122130. Faisalabad, Pakistan: University of Agriculture.Google Scholar
Roose, M. L. & Traugh, S. N. (1988). Identification and performance of citrus trees on nucellar and zygotic rootstocks. Journal of the American Society for Horticultural Science 113, 100105.Google Scholar
Schäfer, G., Bastianel, M. & Dornelles, A. L. C. (2004). Genetic diversity of citrus rootstocks based on RAPD marker analysis. Ciência Rural 34, 14371442.Google Scholar
Shannon, L. M., Frolich, E. F. & Cameron, S. H. (1960). Characteristics of Poncirus trifoliata selections. Proceedings of the American Society for Horticultural Society 76, 163169.Google Scholar
Swingle, W. T. (1967). The botany of Citrus and its wild relatives. In The Citrus Industry, vol. 1 History, World Distribution, Botany and Varieties (Eds Reuther, W., Webber, H. J. & Batchelor, L. D.), pp. 190430. Berkeley, California: University of California.Google Scholar
Tanaka, T. (1961). Citologia: Semi-Centennial Commemoration Papers on Citrus Studies. Osaka, Japan: Citrologia Supporting Foundation.Google Scholar
Uzun, A., Gulsen, O., Kafa, G. & Seday, U. (2009). Field performance and molecular diversification of lemon selections. Scientia Horticulturae 120, 473478.Google Scholar
Uzun, A., Gulsen, O., Seday, U., Yesiloglu, T., Aka-Kacar, Y. & Tuzcu, O. (2011). Investigation of genetic relationships among trifoliata oranges and their hybrid relatives based on ISSR markers. Romanian Biotechnological Letters 16, 64306438.Google Scholar
Weising, K. & Gardner, R. C. (1999). A set of conserved PCR primers for the analysis of simple sequence repeat polymorphisms in chloroplast genomes of dicotyledonous angiosperms. Genome 42, 919.Google Scholar
Wheaton, T. A., Castle, W. S., Whitney, J. D. & Tucker, D. P. H. (1991). Performance of citrus scion cultivars and rootstock in a high-density planting. HortScience 26, 837840.Google Scholar
Wu, G., Wei, Z. K., Wang, Y. X., Chu, L. Y. & Shao, H. B. (2007). The mutual responses of higher plants to environment: physiological and microbiological aspects. Colloids and Surfaces B: Biointerfaces 59, 113119.Google Scholar
Zekri, M. & Al-Jaleel, A. (2004). Evaluation of rootstocks for Valencia and Navel orange trees in Saudi Arabia. Fruits 59, 91100.Google Scholar
Ziegler, L. W. & Wolfe, H. S. (1975). Citrus Growing in Florida. Gainesville, Florida: University of Florida Press.Google Scholar