South Asian Journal of Parasitology

Interspecific Hybridization as a Primary Force in Evolutionary Transformation of Fungi

Asad Nadeem Pasha

Department of Plant Pathology, Bahauddin Zakariya University, Multan, Pakistan.

Umar Imtiaz

Department of Seed Science and Technology, University of Agriculture Faisalabad, Pakistan.

Muhammad Zubair

Department of Plant Pathology, University of Agriculture Faisalabad, Pakistan.

Muhammad Hassan Arif

Department of Seed Science and Technology, University of Agriculture Faisalabad, Pakistan.

Rao Saad Rehman *

College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, Hubei, China.

Sabeen Muntaha

Department of Plant Pathology, University of Agriculture Faisalabad, Pakistan.

Ahsan Amin

Department of Plant Pathology, Bahauddin Zakariya University, Multan, Pakistan.

Aqib Riaz

Department of Plant Pathology, Bahauddin Zakariya University, Multan, Pakistan.

*Author to whom correspondence should be addressed.

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Abstract

Gene transfer across species is often linked to bacteria, which have developed a lot of approaches to promote horizontal DNA exchange. But whole-genome sequencing has shown that fungal species exchange DNA as well, resulting in interwoven lineages, unclear species boundaries, or even the emergence of new species. The interspecific hybridization (IH) that occurs in fungi, as opposed to prokaryote DNA exchange, results in a polyploid genome that is very unstable and quickly develops into more stable derivatives. Genotypic and phenotypic diversity may be combined in creative ways to improve fitness and facilitate the colonization of different habitats in the resultant hybrids. IH led to the formation of major pathogens for plants and humans (for example, numerous "powdery mildew" and Candida species, respectively), as well as important industrial yeasts, including Saccharomyces hybrids that are vital in the manufacturing of cold-cellared Belgian beers and cold-fermented lagers. In this review, we explore the genetic mechanisms and evolutionary consequences of IH in fungi, as well as some of the most well-studied instances of this phenomenon. It's also possible to research the molecular processes that underlie evolution, speciation, and adaptation by using hybrids; this may also lead to the creation of novel varieties for commercial use.

Keywords: Horizontal gene transfer, transcriptome shock, heterosis, interspecific hybridization, reproductive barriers

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References

Griffith F. The significance of pneumococcal types. Epidemiology & Infection. 1928;27(2):113-159.

Riley MA, Lizotte-Waniewski M. Population genomics and the bacterial species concept. Horizontal Gene Transfer. 2009; 367-377.

Stebbins GL. The role of hybridization in evolution. Proceedings of the American Philosophical Society. 1959;103(2):231-251.

Lamichhaney S, Han F, Webster MT, Andersson L, Grant BR, Grant PR. Rapid hybrid speciation in Darwin’s finches. Science. 2018;359(6372):224-228.

Gallone B, Steensels J, Mertens S, Dzialo MC, Gordon JL, Wauters R, Theßeling FA, Bellinazzo F, Saels V, Herrera-Malaver B, Prahl T. Interspecific hybridization facilitates niche adaptation in beer yeast. Nature Ecology & Evolution. 2019;3 (11):1562-1575.

Kominek J, Doering DT, Opulente DA, Shen XX, Zhou X, DeVirgilio J, Hulfachor AB, Groenewald M, Mcgee MA, Karlen SD, Kurtzman CP. Eukaryotic acquisition of a bacterial operon. Cell. 2019;176(6):1356-1366.

Lee SC, Ni M, Li W, Shertz C, Heitman J. The evolution of sex: a perspective from the fungal kingdom. Microbiology and molecular biology reviews. 2010;74(2):298-340.

Idnurm A, James TY, Vilgalys R. Sex in the rest: Mysterious mating in the Chytridiomycota and Zygomycota. Sex in fungi: molecular determination and evolutionary implications. 2007;405-418.

Clutterbuck AJ. Parasexual recombination in fungi. Journal of Genetics. 1996;75 (3):281-286.

Sun D. Pull in and push out: mechanisms of horizontal gene transfer in bacteria. Frontiers in microbiology. 2018;9:2154.

Soltis DE, Visger CJ, Soltis PS. The polyploidy revolution then… and now: Stebbins revisited. American journal of botany. 2014;101(7):1057-1078.

Hübner S, Bercovich N, Todesco M, Mandel JR, Odenheimer J, Ziegler E, Lee JS, Baute GJ, Owens GL, Grassa CJ, Ebert DP. Sunflower pan-genome analysis shows that hybridization altered gene content and disease resistance. Nature plants. 2019;5(1):54-62.

Edelman NB, Frandsen PB, Miyagi M, Clavijo B, Davey J, Dikow RB, García-Accinelli G, Van Belleghem SM, Patterson N, Neafsey DE, Challis R. Genomic architecture and introgression shape a butterfly radiation. Science. 2019;366 (6465):594-599.

Mixão V, Gabaldón T. Hybridization and emergence of virulence in opportunistic human yeast pathogens. Yeast. 2018;35(1):5-20.

Möller M, Stukenbrock EH. Evolution and genome architecture in fungal plant pathogens. Nature Reviews Microbiology. 2017;15(12):756-771.

Routh A, Domitrovic T, Johnson JE. Host RNAs, including transposons, are encapsidated by a eukaryotic single-stranded RNA virus. Proceedings of the National Academy of Sciences. 2012;109 (6):1907-1912.

Coelho MA, Bakkeren G, Sun S, Hood ME, Giraud T. Fungal sex: the Basidiomycota. Microbiology spectrum. 2017;5(3):5- 13.

Bennett RJ. The parasexual lifestyle of Candida albicans. Current opinion in microbiology. 2015;28:10-17.

Rehman RS, Ali M, Zafar SA, Hussain M, Pasha A, Naveed MS, Ahmad M, Waseem M. Abscisic Acid Mediated Abiotic Stress Tolerance in Plants. Asian J. Res. C. Sci. 2022;7(1):1-17.

Rehman RS, Zafar SA, Ali M, Pasha AN, Naveed MS, Waseem M, Raza A. CRISPR-Cas Mediated Genome Editing: A Paradigm Shift towards Sustainable Agriculture and Biotechnology. Asian P. Res. J. 2022;9(1):27-49.

Mallet J. Hybridization, ecological races and the nature of species: Empirical evidence for the ease of speciation. Philosophical Transactions of the Royal Society B: Biological Sciences. 2008;363(1506):2971-2986.

Kiss L, Pintye A, Kovacs GM, Jankovics T, Fontaine MC, Harvey N, Xu X, Nicot PC, Bardin M, Shykoff JA, Giraud T. Temporal isolation explains host‐related genetic differentiation in a group of widespread mycoparasitic fungi. Molecular Ecology. 2011;20(7):1492-1507.

Greig D, Leu JY. Natural history of budding yeast. Current Biology. 2009;19(19):R886-901.

Karlsson M, Nygren K, Johannesson H. The evolution of the pheromonal signal system and its potential role for reproductive isolation in heterothallic Neurospora. Molecular biology and evolution. 2008;25(1):168-178.

Scheele BC, Pasmans F, Skerratt LF, Berger L, Martel AN, Beukema W, Acevedo AA, Burrowes PA, Carvalho T, Catenazzi A, De la Riva I. Amphibian fungal panzootic causes catastrophic and ongoing loss of biodiversity. Science. 2019;363(6434):1459-1463.

O’hanlon SJ, Rieux A, Farrer RA, Rosa GM, Waldman B, Bataille A, Kosch TA, Murray KA, Brankovics B, Fumagalli M, Martin MD. Recent Asian origin of chytrid fungi causing global amphibian declines. Science. 2018;360(6389):621-627.

Greenspan SE, Lambertini C, Carvalho T, James TY, Toledo LF, Haddad CF, Becker CG. Hybrids of amphibian chytrid show high virulence in native hosts. Scientific reports. 2018;8(1):1-10.

Kuehne HA, Murphy HA, Francis CA, Sniegowski PD. Allopatric divergence, secondary contact, and genetic isolation in wild yeast populations. Current Biology. 2007;17(5):407-411.

Turner E, Jacobson DJ, Taylor JW. Reinforced postmating reproductive isolation barriers in Neurospora, an Ascomycete microfungus. Journal of evolutionary biology. 2010;23(8):1642-1656.

Brasier C. The rise of the hybrid fungi. Nature. 2000;405(6783):134-135.

Giraud T, Yockteng R, López-Villavicencio M, Refrégier G, Hood ME. Mating system of the anther smut fungus Microbotryum violaceum: selfing under heterothallism. Eukaryotic Cell. 2008;7 (5):765-775.

Grabenstein KC, Taylor SA. Breaking barriers: causes, consequences, and experimental utility of human-mediated hybridization. Trends Ecol. Evol. 2018; 33:198–212.

Fisher MC, Henk D, Briggs CJ, Brownstein JS, Madoff LC, McCraw SL, Gurr SJ. Emerging fungal threats to animal, plant and ecosystem health. Nature. 2012;484 (7393):186-194.

Wallace AR. Darwinism: an exposition of the theory of natural selection with some of its applications. Cosimo, Inc; 2007.

Giraud T, Gourbiere S. The tempo and modes of evolution of reproductive isolation in fungi. Heredity. 2012;09(4):204-214.

Gac ML, Giraud T. Existence of a pattern of reproductive character displacement in Homobasidiomycota but not in Ascomycota. Journal of evolutionary biology. 2008;21(3):761-772.

Dujon BA, Louis EJ. Genome diversity and evolution in the budding yeasts (Saccharomycotina). Genetics. 2017;206 (2):717-750.

Dettman JR, Sirjusingh C, Kohn LM, Anderson JB. Incipient speciation by divergent adaptation and antagonistic epistasis in yeast. Nature. 2007;447 (7144):585-588.

Rehman RS, Zafar SA, Ali M, Ahmad M, Pasha AN, Waseem M, Hafeez AH, Raza A. Plant Pan-genomes: A New Frontier in Understanding Genomic Diversity in Plants. J. Adv. Bio. Biotech. 2022;25(1):10-22.

Charron G, Marsit S, Hénault M, Martin H, Landry CR. Spontaneous whole-genome duplication restores fertility in interspecific hybrids. Nature communications. 2019;10 (1):1-10.

Wolfe KH. Origin of the yeast whole-genome duplication. PLoS biology. 2015;13(8):e1002221.

Leducq JB, Nielly-Thibault L, Charron G, Eberlein C, Verta JP, Samani P, Sylvester K, Hittinger CT, Bell G, Landry CR. Speciation driven by hybridization and chromosomal plasticity in a wild yeast. Nature Microbiology. 2016;1(1):1-10.

Bar-Zvi D, Lupo O, Levy AA, Barkai N. Hybrid vigor: The best of both parents, or a genomic clash? Curr. Opin. Syst. Biol. 2017;6:22–27.

Carlborg Ö, Haley CS. Epistasis: Too often neglected in complex trait studies?. Nature Reviews Genetics. 2004;5(8):618-625.

Herbst RH, Bar-Zvi D, Reikhav S, Soifer I, Breker M, Jona G, Shimoni E, Schuldiner M, Levy AA, Barkai N. Heterosis as a consequence of regulatory incompatibility. BMC biology. 2017;15(1):1-5.

Tirosh I, Reikhav S, Levy AA, Barkai N. A yeast hybrid provides insight into the evolution of gene expression regulation. Science. 2009;324(5927):659-662.

Feurtey A, Stevens DM, Stephan W, Stukenbrock EH. Interspecific gene exchange introduces high genetic variability in crop pathogen. Genome Biology and Evolution. 2019;11(11):3095-3105.

Corcoran P, Anderson JL, Jacobson DJ, Sun Y, Ni P, Lascoux M, Johannesson H. Introgression maintains the genetic integrity of the mating-type determining chromosome of the fungus Neurospora tetrasperma. Genome research. 2016;26 (4):486-498.

Rehman RS, Pasha AN, Zafar SA, Ali M, Waseem M, Ahmad M, Ahmad N, Hafeez AH. Chromosomal Engineering through CRISPR/Cas Technology: A Way Forward. J. Adv. Bio. Biotech. 2022;25(1):34-45.

Rehman RS, Ali M, Zafar SA, Ahmad M, Pasha AN, Bashir H, Rashid F, Hussain M. Tapping into the Unsung Potential of CRISPR/CAS Technology in Agriculture. Asian J. Biochem. Gen. Mol. Bio. 2022;10 (4):1-26.

Hussain A, Bashir H, Zafar SA, Rehman RS, Khalid MN, Awais M, Sadiq M, Amjad I. The importance of soil organic matter (SOM) on soil productivity and plant growth. Biological and Agricultural Sciences Research Journal. 2023;(1):11-11.

Magwene PM, Kayıkçı Ö, Granek JA, Reininga JM, Scholl Z, Murray D. Outcrossing, mitotic recombination, and life-history trade-offs shape genome evolution in Saccharomyces cerevisiae. Proceedings of the National Academy of Sciences. 2011;108(5):1987-1992.

Pryszcz LP, Németh T, Saus E, Ksiezopolska E, Hegedűsová E, Nosek J, Wolfe KH, Gacser A, Gabaldón T. The genomic aftermath of hybridization in the opportunistic pathogen Candida metapsilosis. PLoS genetics. 2015;11 (10):e1005626.

Vishnoi A, Sethupathy P, Simola D, Plotkin JB, Hannenhalli S. Genome-wide survey of natural selection on functional, structural, and network properties of polymorphic sites in Saccharomyces paradoxus. Molecular biology and evolution. 2011; 28(9):2615-2627.

Bashir H, Zafar SA, Rehman RS, Hussain M, Haris M, Khalid MN, Awais M, Sadiq M, Amjad I. Impact of potentially soil mineralizable nitrogen (pmn) on soil health and crop production. Biological and Agricultural Sciences Research Journal. 2023;(1).

Taylor SA, Larson EL. Insights from genomes into the evolutionary importance and prevalence of hybridization in nature. Nature ecology & evolution. 2019;3(2):170-177.

Smukowski Heil CS, DeSevo CG, Pai DA, Tucker CM, Hoang ML, Dunham MJ. Loss of heterozygosity drives adaptation in hybrid yeast. Molecular biology and evolution. 2017;34(7):1596-1612.

Zhang Z, Bendixsen DP, Janzen T, Nolte AW, Greig D, Stelkens R. Recombining your way out of trouble: the genetic architecture of hybrid fitness under environmental stress. Molecular biology and evolution. 2020;37(1):167-182.

Smukowski Heil CS, Large CR, Patterson K, Hickey AS, Yeh CL, Dunham MJ. Temperature preference can bias parental genome retention during hybrid evolution. PLoS genetics. 2019;15(9):e1008383.

Mixão V, Gabaldón T. Genomic evidence for a hybrid origin of the yeast opportunistic pathogen Candida albicans. BMC biology. 2020;18(1):1-4.

Ford CB, Funt JM, Abbey D, Issi L, Guiducci C, Martinez DA, Delorey T, yu Li B, White TC, Cuomo C, Rao RP. The evolution of drug resistance in clinical isolates of Candida albicans. elife. 2015;4:e00662.

Selmecki AM, Maruvka YE, Richmond PA, Guillet M, Shoresh N, Sorenson AL, De S, Kishony R, Michor F, Dowell R, Pellman D. Polyploidy can drive rapid adaptation in yeast. Nature. 2015;519(7543):349-352.

Yang F, Teoh F, Tan AS, Cao Y, Pavelka N, Berman J. Aneuploidy enables cross-adaptation to unrelated drugs. Molecular biology and evolution. 2019;36(8):1768-1782.

Rehman RS, Zafar SA, Ali M, Pasha AN, Bashir H, Ashraf MA, Yaqoob MU, Hussain M. Biochemical and Molecular Insights into Abiotic Stress Tolerance in Plants. Asian J. Biotech. Gen. Engg. 2022;5(2):1-19.

Hu G, Wang J, Choi J, Jung WH, Liu I, Litvintseva AP, Bicanic T, Aurora R, Mitchell TG, Perfect JR, Kronstad JW. Variation in chromosome copy number influences the virulence of Cryptococcus neoformans and occurs in isolates from AIDS patients. BMC genomics. 2011;12 (1):1-9.

Basse CW. Mitochondrial inheritance in fungi. Current opinion in microbiology. 2010;13(6):712-719.

Olson Å, Stenlid J. Mitochondrial control of fungal hybrid virulence. Nature. 2001;411 (6836):438-440.

Giordano L, Sillo F, Garbelotto M, Gonthier P. Mitonuclear interactions may contribute to fitness of fungal hybrids. Sci. Rep. 2018;8:1706.

Barr CM, Neiman M, Taylor DR. Inheritance and recombination of mitochondrial genomes in plants, fungi and animals. New Phytol. 2005;168:39–50.

Chou JY, Hung YS, Lin KH, Lee HY, Leu JY. Multiple molecular mechanisms cause reproductive isolation between three yeast species. PLoS Biol. 2010;8:e1000432.

Olson Å, Stenlid J. Mitochondrial control of fungal hybrid virulence. Nature. 2001;411(6836):438-440.

Rehman RS, Khan K, Zafar SA, Pasha AN, Ali M, Ashraf MA, Bashir H, Rashid F. Character Association Studies in Various Brassica napus Genotypes under Drought Stress. Asian J. Res. Bot. 2022;7(2):20-27.

Jhuang HY, Lee HY, Leu JY. Mitochondrial–nuclear co‐evolution leads to hybrid incompatibility through pentatricopeptide repeat proteins. EMBO reports. 2017;18(1):87-101.

Baker E, Wang B, Bellora N, Peris D, Hulfachor AB, Koshalek JA, Adams M, Libkind D, Hittinger CT. The genome sequence of Saccharomyces eubayanus and the domestication of lager-brewing yeasts. Molecular biology and evolution. 2015;32(11):2818-2831.

Li XC, Peris D, Hittinger CT, Sia EA, Fay JC. Mitochondria-encoded genes contribute to evolution of heat and cold tolerance in yeast. Science advances. 2019;5(1):18-48.

Yoo MJ, Liu X, Pires JC, Soltis PS, Soltis DE. Nonadditive gene expression in polyploids. Annu Rev Genet. 2014;48(1):485-517.

Bird KA, VanBuren R, Puzey JR, Edger PP. The causes and consequences of subgenome dominance in hybrids and recent polyploids. New Phytologist. 2018;220(1):87-93.

De Smet R, Van de Peer Y. Redundancy and rewiring of genetic networks following genome-wide duplication events. Current opinion in plant biology. 2012;15(2):168-176.

Rehman RS, Pasha AN, Zafar SA, Ali M, Bashir H, Saeed MU, Ashraf NA, Javed A. Molecular Mechanisms behind the Regulation of Rice Tiller Angle: An Update. Asian J. Biol. 2022;14(4):37-50.

Rehman RS, Ali M, Zafar SA, Bashir H, Pasha AN, Javed A, Ashraf NA, Shah WA. Regulatory Role of DNA Methylation and Its Significance in Plants. Asian J. Biochem. Gen. Mol. Bio. 2022;11(3):1-15.

Cox MP, Dong T, Shen G, Dalvi Y, Scott DB, Ganley AR. An interspecific fungal hybrid reveals cross-kingdom rules for allopolyploid gene expression patterns. PLoS genetics. 2014;10(3):e1004180.

Olesen K, Felding T, Gjermansen C, Hansen J. The dynamics of the Saccharomyces carlsbergensis brewing yeast transcriptome during a production-scale lager beer fermentation. FEMS yeast research. 2002;2(3):563-573.

Rehman RS, Hussain M, Ali M, Zafar SA, Pasha AN, Bashir H, Ashraf NA, Javed A, Shah WA. A Comprehensive Review on Melatonin Compound and its Functions in Different Fungi and Plants. Intern. J. Pathogen Res. 2022;10(2):9-21.

Sriswasdi S, Takashima M, Manabe RI, Ohkuma M, Sugita T, Iwasaki W. Global deceleration of gene evolution following recent genome hybridizations in fungi. Genome research. 2016;26(8):1081-1090.

Hovhannisyan H, Saus E, Ksiezopolska E, Gabaldón T. The transcriptional aftermath in two independently formed hybrids of the opportunistic pathogen Candida orthopsilosis. Msphere. 2020;5(3):e00282-20.

Kellis M, Patterson N, Endrizzi M, Birren B, Lander ES. Sequencing and comparison of yeast species to identify genes and regulatory elements. Nature. 2003;423(6937):241-254.

Yoo MJ, Szadkowski E, Wendel JF. Homoeolog expression bias and expression level dominance in allopolyploid cotton. Heredity. 2013;110(2):171-180.

Tirosh I, Barkai N. Inferring regulatory mechanisms from patterns of evolutionary divergence. Molecular systems biology. 2011;7(1):530.

Zafar SA, Aslam M, Khan HZ, Sarwar S, Rehman RS, Hassan M, Ahmad RM, Gill RA, Ali B, Al-Ashkar I, Ibrahim A. Estimation of Genetic Divergence and Character Association Studies in Local and Exotic Diversity Panels of Soybean (Glycine max L.) Genotypes. Phyton-Intern. J. Exp. Bot. 2023;92(6):1887-1906.

Yang B, Wittkopp PJ. Structure of the transcriptional regulatory network correlates with regulatory divergence in Drosophila. Molecular biology and evolution. 2017;34(6):1352-1362.

Dunn B, Paulish T, Stanbery A, Piotrowski J, Koniges G, Kroll E, Louis EJ, Liti G, Sherlock G, Rosenzweig F. Recurrent rearrangement during adaptive evolution in an interspecific yeast hybrid suggests a model for rapid introgression. PLoS genetics. 2013;9(3):e1003366.

Rehman RS, Zafar SA, Ali M, Bxashir H, Pasha AN. Regulatory Role of Nucleus in miRNA Processing at Early Developmental Stages in Plants. Asian J. Biotech. Gen. Engg. 2022;5(4):8-11.

Monerawela C, James TC, Wolfe KH, Bond U. Loss of lager specific genes and subtelomeric regions define two different Saccharomyces cerevisiae lineages for Saccharomyces pastorianus Group I and II strains. FEMS Yeast Research. 2015;15(2):fou008.

Li XC, Fay JC. Cis-regulatory divergence in gene expression between two thermally divergent yeast species. Genome biology and evolution. 2017;9(5):1120-1129.

Christiaens JF, Van Mulders SE, Duitama J, Brown CA, Ghequire MG, De Meester L, Michiels J, Wenseleers T, Voordeckers K, Verstrepen KJ. Functional divergence of gene duplicates through ectopic recombination. EMBO reports. 2012;13(12):1145-1151.

Hewitt SK, Donaldson IJ, Lovell SC, Delneri D. Sequencing and characterisation of rearrangements in three S. pastorianus strains reveals the presence of chimeric genes and gives evidence of breakpoint reuse. PLoS one. 2014;9(3):e92203.

Dandage R, Berger CM, Gagnon-Arsenault I, Moon KM, Stacey RG, Foster LJ, Landry CR. Frequent assembly of chimeric complexes in the protein interaction network of an interspecies yeast hybrid. Molecular biology and evolution. 2021;38 (4):1384-1401.

Leducq JB, Charron G, Diss G, Gagnon-Arsenault I, Dubé AK, Landry CR. Evidence for the robustness of protein complexes to inter-species hybridization. PLoS genetics. 2012;8(12):e1003161.

Piatkowska EM, Naseeb S, Knight D, Delneri D. Chimeric protein complexes in hybrid species generate novel phenotypes. PLoS genetics. 2013;9(10):e1003836.

Zamir L, Zaretsky M, Fridman Y, Ner-Gaon H, Rubin E, Aharoni A. Tight coevolution of proliferating cell nuclear antigen (PCNA)-partner interaction networks in fungi leads to interspecies network incompatibility. Proceedings of the National Academy of Sciences. 2012;109(7):E406-414.

Hornsey IS. A history of beer and brewing. Royal Society of Chemistry; 2003.

Steensels J, Gallone B, Voordeckers K, Verstrepen KJ. Domestication of industrial microbes. Current biology. 2019;29(10): R381-393.

Gallone B, Mertens S, Gordon JL, Maere S, Verstrepen KJ, Steensels J. Origins, evolution, domestication and diversity of Saccharomyces beer yeasts. Current opinion in biotechnology. 2018;49:148-155.

Salazar AN, Gorter de Vries AR, Van Den Broek M, Brouwers N, de la Torre Cortès P, Kuijpers NG, Daran JM, Abeel T. Chromosome level assembly and comparative genome analysis confirm lager-brewing yeasts originated from a single hybridization. BMC genomics. 2019;20(1):1-18.

Steensels J, Snoek T, Meersman E, Nicolino MP, Voordeckers K, Verstrepen KJ. Improving industrial yeast strains: exploiting natural and artificial diversity. FEMS microbiology reviews. 2014;38(5):947-995.

Bashir H, Zafar SA, Rehman RS, Khalid MN, Amjad I. Breeding potential of sesame for waterlogging stress in Asia. Biological and Agricultural Sciences Research Journal. 2023;(1):10-10.

Dzialo MC, Park R, Steensels J, Lievens B, Verstrepen KJ. Physiology, ecology and industrial applications of aroma formation in yeast. FEMS microbiology reviews. 2017;41:S95-128.

Goold HD, Kroukamp H, Williams TC, Paulsen IT, Varela C, Pretorius IS. Yeast's balancing act between ethanol and glycerol production in low‐alcohol wines. Microbial biotechnology. 2017;10(2):264-278.

Bellon JR, Schmid F, Capone DL, Dunn BL, Chambers PJ. Introducing a new breed of wine yeast: interspecific hybridisation between a commercial Saccharomyces cerevisiae wine yeast and Saccharomyces mikatae. PLoS one. 2013;8(4):e62053.

Jetti KD, Gns RR, Garlapati D, Nammi SK. Improved ethanol productivity and ethanol tolerance through genome shuffling of Saccharomyces cerevisiae and Pichia stipitis. International Microbiology. 2019;22(2):247-254.

Peris D, Alexander WG, Fisher KJ, Moriarty RV, Basuino MG, Ubbelohde EJ, Wrobel RL, Hittinger CT. Synthetic hybrids of six yeast species. Nature communications. 2020;11(1):1-11.

Depotter JR, Seidl MF, Wood TA, Thomma BP. Interspecific hybridization impacts host range and pathogenicity of filamentous microbes. Current Opinion in Microbiology. 2016 Aug 1;32:7-13.

Brasier CM, Cooke DE, Duncan JM. Origin of a new Phytophthora pathogen through interspecific hybridization. Proceedings of the National Academy of Sciences. 1999;96(10):5878-5883.

Hessenauer P, Fijarczyk A, Martin H, Prunier J, Charron G, Chapuis J, Bernier L, Tanguay P, Hamelin RC, Landry CR. Hybridization and introgression drive genome evolution of Dutch elm disease pathogens. Nature ecology & evolution. 2020;4(4):626-638.

Steenwyk JL, Lind AL, Ries LN, Dos Reis TF, Silva LP, Almeida F, Bastos RW, Bonato VL, Pessoni AM, Rodrigues F, Raja HA. Pathogenic allodiploid hybrids of Aspergillus fungi. Current Biology. 2020;30(13):2495-2507.

Pfaller MA, Diekema D. Epidemiology of invasive candidiasis: A persistent public health problem. Clinical microbiology reviews. 2007;20(1):133-163.

Ropars J, Maufrais C, Diogo D, Marcet-Houben M, Perin A, Sertour N, Mosca K, Permal E, Laval G, Bouchier C, Ma L. Gene flow contributes to diversification of the major fungal pathogen Candida albicans. Nature communications. 2018;9(1):1-10.

Mixão V, Hansen AP, Saus E, Boekhout T, Lass-Florl C, Gabaldón T. Whole-genome sequencing of the opportunistic yeast pathogen Candida inconspicua uncovers its hybrid origin. Frontiers in genetics. 2019;10:383.

Rehman RS, Khan K, Zaka A, Ali M, Ahmad N, Zaghum J, Umar M, Arham A, Anwar U. Effect of topping under different nitrogen levels on agronomic characters of cotton. The International Journal of Biological Research. 2019;2:1-10.

Schröder MS, Martinez de San Vicente K, Prandini TH, Hammel S, Higgins DG, Bagagli E, Wolfe KH, Butler G. Multiple origins of the pathogenic yeast Candida orthopsilosis by separate hybridizations between two parental species. PLoS genetics. 2016;12(11):e1006404.

Imran A, Saleem MB, Anwer A, Rehman RS, Naeem M, Hafeez MF, Shah AJ. Genetic divergence of Bt cotton (Gossypium hirsutum L.) Germplasm based on principal component analysis. Nature and Science. 2017;15:11.

Wicker T, Oberhaensli S, Parlange F, Buchmann JP, Shatalina M, Roffler S, Ben-David R, Doležel J, Šimková H, Schulze-Lefert P, Spanu PD. The wheat powdery mildew genome shows the unique evolution of an obligate biotroph. Nature genetics. 2013;45(9):1092-1096.

Menardo F, Praz CR, Wyder S, Ben-David R, Bourras S, Matsumae H, McNally KE, Parlange F, Riba A, Roffler S, Schaefer LK. Hybridization of powdery mildew strains gives rise to pathogens on novel agricultural crop species. Nature Genetics. 2016;48(2):201-205.

Walker AS, Bouguennec A, Confais J, Morgant G, Leroux P. Evidence of host‐range expansion from new powdery mildew (Blumeria graminis) infections of triticale (× Triticosecale) in France. Plant Pathology. 2011;60(2):207-220.

Troch V, Audenaert K, Bekaert B, Höfte M, Haesaert G. Phylogeography and virulence structure of the powdery mildew population on its' new'host triticale. BMC Evolutionary Biology. 2012;12(1):1-12.

Shen XX, Opulente DA, Kominek J, Zhou X, Steenwyk JL, Buh KV, Haase MA, Wisecaver JH, Wang M, Doering DT, Boudouris JT. Tempo and mode of genome evolution in the budding yeast subphylum. Cell. 2018;175(6):1533- 1545.

Rehman RS, Bashir H, Zafar SA, Ali M, Javed A, Ashraf NA, Hussain M, Hussain A. A Comprehensive Review on Cytoskeletal Organization and Its Interaction with Polysaccharides and Enzymes during Primary Cell Wall Development. Biotechnology Journal International. 2022;26(4):11-28.

Dujon B. Yeasts illustrate the molecular mechanisms of eukaryotic genome evolution. TRENDS in Genetics. 2006;22 (7):375-387.

Gryganskyi AP, Golan J, Dolatabadi S, Mondo S, Robb S, Idnurm A, Muszewska A, Steczkiewicz K, Masonjones S, Liao HL, Gajdeczka MT. Phylogenetic and phylogenomic definition of Rhizopus species. G3: Genes, Genomes, Genetics. 2018;8(6):2007-2018.

Wu G, Zhao H, Li C, Rajapakse MP, Wong WC, Xu J, Saunders CW, Reeder NL, Reilman RA, Scheynius A, Sun S. Genus-wide comparative genomics of Malassezia delineates its phylogeny, physiology, and niche adaptation on human skin. PLoS genetics. 2015;11(11):e1005614.

Bovers M, Hagen F, Kuramae EE, Diaz MR, Spanjaard L, Dromer F, Hoogveld HL, Boekhout T. Unique hybrids between the fungal pathogens Cryptococcus neoformans and Cryptococcus gattii. FEMS yeast research. 2006;6(4):599-607.

Libkind D, Hittinger CT, Valério E, Gonçalves C, Dover J, Johnston M, Gonçalves P, Sampaio JP. Microbe domestication and the identification of the wild genetic stock of lager-brewing yeast. Proceedings of the National Academy of Sciences. 2011;108(35):14539-14544.

Pérez-Través L, Lopes CA, Querol A, Barrio E. On the complexity of the Saccharomyces bayanus taxon: hybridization and potential hybrid speciation. PLoS one. 2014;9(4):e93729.

Borneman AR, Zeppel R, Chambers PJ, Curtin CD. Insights into the Dekkera bruxellensis genomic landscape: comparative genomics reveals variations in ploidy and nutrient utilisation potential amongst wine isolates. PLoS genetics. 2014;10(2):e1004161.

Ahmad N, Rehman RS, Ali M, Arham A, Zaka A, Shafiq Y, Zaghum J, Raza A, Hasnain N. Heterosis studies of yield and fiber quality traits in Gossypium hirsutum L. The International Journal of Biological Research. 2019;2:1-13.

Saubin M, Devillers H, Proust L, Brier C, Grondin C, Pradal M, Legras JL, Neuvéglise C. Investigation of genetic relationships between Hanseniaspora species found in grape musts revealed interspecific hybrids with dynamic genome structures. Frontiers in microbiology. 2020;10:2960.

Neafsey DE, Barker BM, Sharpton TJ, Stajich JE, Park DJ, Whiston E, Hung CY, McMahan C, White J, Sykes S, Heiman D. Population genomic sequencing of Coccidioides fungi reveals recent hybridization and transposon control. Genome research. 2010;20(7):938-946.

Staats M, Van Baarlen P, van Kan JA. Molecular phylogeny of the plant pathogenic genus Botrytis and the evolution of host specificity. Molecular biology and Evolution. 2005;22(2):333-346.

Inderbitzin P, Davis RM, Bostock RM, Subbarao KV. The ascomycete Verticillium longisporum is a hybrid and a plant pathogen with an expanded host range. PloS one. 2011;6(3):e18260.

Nikulin J, Krogerus K, Gibson B. Alternative Saccharomyces interspecies hybrid combinations and their potential for low‐temperature wort fermentation. Yeast. 2018;35(1):113-127.

Magalhães F, Krogerus K, Vidgren V, Sandell M, Gibson B. Improved cider fermentation performance and quality with newly generated Saccharomyces cerevisiae× Saccharomyces eubayanus hybrids. Journal of Industrial Microbiology and Biotechnology. 2017;44(8):1203-1213.

Ashraf NA, Javed A, Rehman RS, Azhar A. Agro-morphological response of different okra (Abelmoschus esculentus L.) genotypes and their F1 crosses under waste water and normal irrigation treatments. Journal of Agricultural and Basic Sciences; 2021.

Peris D, Moriarty RV, Alexander WG, Baker E, Sylvester K, Sardi M, Langdon QK, Libkind D, Wang QM, Bai FY, Leducq JB. Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production. Biotechnology for Biofuels. 2017;10(1):1-9.

Winans MJ, Yamamoto Y, Fujimaru Y, Kusaba Y, Gallagher JE, Kitagaki H. Saccharomyces arboricola and Its hybrids’ propensity for sake production: interspecific hybrids reveal increased fermentation abilities and a mosaic metabolic profile. Fermentation. 2020;6 (1):14.

Varavallo MA, Queiroz MV, Lana TG, Brito AT, Gonçalves DB, Araújo EF. Isolation of recombinant strains with enhanced pectinase production by protoplast fusion between Penicillium expansum and Penicillium griseoroseum. Brazilian Journal of Microbiology. 2007;38:52-57.

Kaur B, Oberoi HS, Chadha BS. Enhanced cellulase producing mutants developed from heterokaryotic Aspergillus strain. Bioresource technology. 2014;156:100-107.

Guo X, Wang R, Chen Y, Xiao D. Intergeneric yeast fusants with efficient ethanol production from cheese whey powder solution: Construction of a Kluyveromyces marxianus and Saccharomyces cerevisiae AY‐5 hybrid. Engineering in Life Sciences. 2012;12(6):656-661.

Ye M, Yue T, Yuan Y, Wang L. Production of yeast hybrids for improvement of cider by protoplast electrofusion. Biochemical engineering journal. 2013;81:162-169.

Patil NS, Patil SM, Govindwar SP, Jadhav JP. Molecular characterization of intergeneric hybrid between Aspergillus oryzae and Trichoderma harzianum by protoplast fusion. Journal of applied microbiology. 2015;118(2):390-398.