1932

Abstract

Wheat is the predominant crop worldwide, contributing approximately 20% of protein and calories to the human diet. However, the yield potential of wheat faces limitations due to pests, diseases, and abiotic stresses. Although conventional breeding has improved desirable traits, the use of modern transgenesis technologies has been limited in wheat in comparison to other crops such as maize and soybean. Recent advances in wheat gene cloning and transformation technology now enable the development of a super wheat consistent with the One Health goals of sustainability, food security, and environmental stewardship. This variety combines traits to enhance pest and disease resistance, elevate grain nutritional value, and improve resilience to climate change. In this review, we explore ways to leverage current technologies to combine and transform useful traits into wheat. We also address the requirements of breeders and legal considerations such as patents and regulatory issues.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-phyto-121423-042128
2024-09-09
2024-10-15
Loading full text...

Full text loading...

/deliver/fulltext/phyto/62/1/annurev-phyto-121423-042128.html?itemId=/content/journals/10.1146/annurev-phyto-121423-042128&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Alhanti B, van Wendel de Joode B, Martinez MS, Mora AM, Gamboa LC, et al. 2022.. Environmental exposures contribute to respiratory and allergic symptoms among women living in the banana growing regions of Costa Rica. . Occup. Environ. Med. 79:(7):46976
    [Crossref] [Google Scholar]
  2. 2.
    Araus JL, Serret MD, Lopes MS. 2019.. Transgenic solutions to increase yield and stability in wheat: shining hope or flash in the pan?. J. Exp. Bot. 70:(5):141924
    [Crossref] [Google Scholar]
  3. 3.
    Argos P, Landy A, Abremski K, Egan JB, Haggard-Ljungquist E, et al. 1986.. The integrase family of site-specific recombinases: regional similarities and global diversity. . EMBO J. 5:(2):43340
    [Crossref] [Google Scholar]
  4. 4.
    Arndell T, Chen J, Sperschneider J, Upadhyaya NM, Blundell C, et al. 2023.. Pooled effector library screening in protoplasts rapidly identifies novel Avr genes. . bioRxiv 538616. https://doi.org/10.1101/2023.04.28.538616
  5. 5.
    Arora S, Steed A, Goddard R, Gaurav K, O'Hara T, et al. 2023.. A wheat kinase and immune receptor form host-specificity barriers against the blast fungus. . Nat. Plants 9:(3):38592
    [Crossref] [Google Scholar]
  6. 6.
    Arora S, Steuernagel B, Gaurav K, Chandramohan S, Long Y, et al. 2019.. Resistance gene cloning from a wild crop relative by sequence capture and association genetics. . Nat. Biotechnol. 37:(2):13943
    [Crossref] [Google Scholar]
  7. 7.
    Arranz-Otaegui A, Carretero LG, Ramsey MN, Fuller DQ, Richter T. 2018.. Archaeobotanical evidence reveals the origins of bread 14,400 years ago in northeastern Jordan. . PNAS 115:(31):792530
    [Crossref] [Google Scholar]
  8. 8.
    Arumuganathan K, Earle ED. 1991.. Nuclear DNA content of some important plant species. . Plant Mol. Biol. Rep. 9:(3):20818
    [Crossref] [Google Scholar]
  9. 9.
    Assoc. for Molecular Pathology v. Myriad Genetics, Inc., 569 U.S. 576 ( 2013.)
  10. 10.
    Athiyannan N, Abrouk M, Boshoff WHP, Cauet S, Rodde N, et al. 2022.. Long-read genome sequencing of bread wheat facilitates disease resistance gene cloning. . Nat. Genet. 54:(3):22731
    [Crossref] [Google Scholar]
  11. 11.
    Bakala HS, Mandahal KS, Ankita Sarao LK, Srivastava P. 2022.. Breeding wheat for biotic stress resistance: achievements, challenges and prospects. . InTechOpen. http://dx.doi.org/10.5772/intechopen.97359
    [Google Scholar]
  12. 12.
    Balk J, Connorton JM, Wan Y, Lovegrove A, Moore KL, et al. 2019.. Improving wheat as a source of iron and zinc for global nutrition. . Nutr. Bull. 44:(1):5359
    [Crossref] [Google Scholar]
  13. 13.
    Barfield CE, Calfee JE. 2007.. Biotechnology and the patent system: balancing innovation and property rights. Rep. , Am. Enterp. Inst., Washington, DC:. https://www.aei.org/wp-content/uploads/2013/12/-biotechnology-and-the-patent-system-book_121440333605.pdf
    [Google Scholar]
  14. 14.
    Barroso PAV. 2023.. NOTA sobre a liberação comercial para plantio do trigo IND-ØØ412–7 (HB4). Rep. , CTNBio, Brasilia:. http://ctnbio.mctic.gov.br/documents/566540/0/Nota+T%C3%A9cnica_Trigo_HB4+2.pdf
    [Google Scholar]
  15. 15.
    Becker D, Wieser W, Koehler P, Folck A, Mühling KH, Zörb C. 2012.. Protein composition and techno-functional properties of transgenic wheat with reduced α-gliadin content obtained by RNA interference. . J. Appl. Bot. Food Q. 85::2333
    [Google Scholar]
  16. 16.
    Beker MP, Boari P, Burachik M, Cuadrado V, Junco M, et al. 2016.. Development of a construct-based risk assessment framework for genetic engineered crops. . Transgenic Res. 25:(5):597607
    [Crossref] [Google Scholar]
  17. 17.
    Bent AF, Kunkel BN, Dahlbeck D, Brown KL, Schmidt R, et al. 1994.. RPS2 of Arabidopsis thaliana: a leucine-rich repeat class of plant disease resistance genes. . Science 265:(5180):185660
    [Crossref] [Google Scholar]
  18. 18.
    Berzonsky WA, Ding H, Haley SD, Harris MO, Lamb RJ, et al. 2003.. Breeding wheat for resistance to insects. . Plant Breed. Rev. 22::22196
    [Google Scholar]
  19. 19.
    Beznec A, Faccio P, Miralles DJ, Abeledo LG, Oneto CD, et al. 2021.. Stress-induced expression of IPT gene in transgenic wheat reduces grain yield penalty under drought. . J. Genet. Eng. Biotechnol. 19:(1):67
    [Crossref] [Google Scholar]
  20. 20.
    Borrill P, Harrington SA, Uauy C. 2019.. Applying the latest advances in genomics and phenomics for trait discovery in polyploid wheat. . Plant J. 97:(1):5672
    [Crossref] [Google Scholar]
  21. 21.
    Brabham HJ, Hernández-Pinzón I, Yanagihara C, Ishikawa N, Komori T, et al. 2023.. Rapid discovery of functional NLRs using the signature of high expression, high-throughput transformation, and large-scale phenotyping. . Cell. In press
    [Google Scholar]
  22. 22.
    Brinch-Pedersen H, Hatzack F, Stöger E, Arcalis E, Pontopidan K, Holm PB. 2006.. Heat-stable phytases in transgenic wheat (Triticum aestivum L.): deposition pattern, thermostability, and phytate hydrolysis. . J. Agric. Food Chem. 54:(13):462432
    [Crossref] [Google Scholar]
  23. 23.
    Cavalet-Giorsa E, González-Muñoz A, Athiyannan N, Holden S, Salhi A, et al. 2023.. Origin and evolution of the bread wheat D genome. . bioRxiv 568958. https://doi.org/10.1101/2023.11.29.568958
  24. 24.
    CDC. 2023.. About One Health. . CDC. https://www.cdc.gov/onehealth/basics/index.html
    [Google Scholar]
  25. 25.
    Chen H, Neubauer M, Wang JP. 2022.. Enhancing HR frequency for precise genome editing in plants. . Front. Plant Sci. 13::883421
    [Crossref] [Google Scholar]
  26. 26.
    Chen R, Gajendiran K, Wulff BBH. 2024.. R we there yet? Advances in cloning resistance genes for engineering immunity in crop plants. . Curr. Opin. Plant Biol. 77::102489
    [Crossref] [Google Scholar]
  27. 27.
    Cheo DL, Titus SA, Byrd DRN, Hartley JL, Temple GF, Brasch MA. 2004.. Concerted assembly and cloning of multiple DNA segments using in vitro site-specific recombination: functional analysis of multi-segment expression clones. . Genome Res. 14:(10B):211120
    [Crossref] [Google Scholar]
  28. 28.
    Dawe RK, Gent JI, Zeng Y, Zhang H, Fu F-F, et al. 2023.. Synthetic maize centromeres transmit chromosomes across generations. . Nat. Plants 9:(3):43341
    [Crossref] [Google Scholar]
  29. 29.
    Debernardi JM, Tricoli DM, Ercoli MF, Hayta S, Ronald P, et al. 2020.. A GRF–GIF chimeric protein improves the regeneration efficiency of transgenic plants. . Nat. Biotechnol. 38:(11):127479
    [Crossref] [Google Scholar]
  30. 30.
    Deising HB, Reimann S, Pascholati SF. 2008.. Mechanisms and significance of fungicide resistance. . Braz. J. Microbiol. 39:(2):28695
    [Crossref] [Google Scholar]
  31. 31.
    Delaney B, Goodman RE, Ladics GS. 2017.. Food and feed safety of genetically engineered food crops. . Toxicol. Sci. 162:(2):36171
    [Crossref] [Google Scholar]
  32. 32.
    des Déserts AD, Bouchet S, Sourdille P, Servin B. 2021.. Evolution of recombination landscapes in diverging populations of bread wheat. . Genome Biol. Evol. 13:(8):evab152
    [Crossref] [Google Scholar]
  33. 33.
    Dracatos PM, Lu J, Sánchez-Martín J, Wulff BB. 2023.. Resistance that stacks up: engineering rust and mildew disease control in the cereal crops wheat and barley. . Plant Biotechnol. J. 21:(10):193851
    [Crossref] [Google Scholar]
  34. 34.
    Edlinger A, Garland G, Hartman K, Banerjee S, Degrune F, et al. 2022.. Agricultural management and pesticide use reduce the functioning of beneficial plant symbionts. . Nat. Ecol. Evol. 6:(8):114554
    [Crossref] [Google Scholar]
  35. 35.
    EFSA. 2010.. Panel on genetically modified organisms (GMO). Scientific opinion on the assessment of potential impacts of genetically modified plants on non-target organisms. . EFSA J. 8:(11):1877
    [Crossref] [Google Scholar]
  36. 36.
    Engler C, Kandzia R, Marillonnet S. 2008.. A one pot, one step, precision cloning method with high throughput capability. . PLOS ONE 3:(11):e3647
    [Crossref] [Google Scholar]
  37. 37.
    Erenstein O, Jaleta M, Mottaleb KA, Sonder K, Donovan J, Braun H-J. 2022.. Wheat Improvement: Food Security in a Changing Climate. Cham, Switz:.: Springer
    [Google Scholar]
  38. 38.
    Foster S, Pulido-Bosch A, Vallejos Á, Molina L, Llop A, MacDonald AM. 2018.. Impact of irrigated agriculture on groundwater-recharge salinity: a major sustainability concern in semi-arid regions. . Hydrogeol. J. 26:(8):278191
    [Crossref] [Google Scholar]
  39. 39.
    Fuller DQ, Stevens CJ. 2019.. Between domestication and civilization: the role of agriculture and arboriculture in the emergence of the first urban societies. . Veg. Hist. Archaeobot. 28:(3):26382
    [Crossref] [Google Scholar]
  40. 40.
    Gantner J, Ordon J, Ilse T, Kretschmer C, Gruetzner R, et al. 2018.. Peripheral infrastructure vectors and an extended set of plant parts for the modular cloning system. . PLOS ONE 13:(5):e0197185
    [Crossref] [Google Scholar]
  41. 41.
    Garcia-Alonso M, Novillo C, Kostolaniova P, Parrilla MM, Alcalde E, Podevin N. 2022.. The EU's GM crop conundrum. . EMBO Rep. 23:(5):e54529
    [Crossref] [Google Scholar]
  42. 42.
    Gaurav K, Arora S, Silva P, Sánchez-Martín J, Horsnell R, et al. 2022.. Population genomic analysis of Aegilops tauschii identifies targets for bread wheat improvement. . Nat. Biotechnol. 40:(3):42231
    [Crossref] [Google Scholar]
  43. 43.
    Gharalari AH, Fox SL, Smith MAH, Lamb RJ. 2009.. Oviposition deterrence in spring wheat, Triticum aestivum, against orange wheat blossom midge, Sitodiplosis mosellana: implications for inheritance of deterrence. . Entomol. Exp. Appl. 133:(1):7483
    [Crossref] [Google Scholar]
  44. 44.
    Gibson DG, Young L, Chuang R-Y, Venter JC, Hutchison CA, Smith HO. 2009.. Enzymatic assembly of DNA molecules up to several hundred kilobases. . Nat. Methods 6:(5):34345
    [Crossref] [Google Scholar]
  45. 45.
    Gil Robles JM, Edlinger R. 1998.. Directive 98/44/EC of the European Parliament and of the Council of 6 July 1998 on the legal protection of biotechnological inventions. . Off. J. Eur. Communities L2134 1::1321
    [Google Scholar]
  46. 46.
    González FG, Capella M, Ribichich KF, Curín F, Giacomelli JI, et al. 2019.. Wheat transgenic plants expressing the sunflower gene HaHB4 significantly outyielded their controls in field trials. . J. Exp. Bot. 70:(5):166981
    [Crossref] [Google Scholar]
  47. 47.
    Guo J, Zhang X, Hou Y, Cai J, Shen X, et al. 2015.. High-density mapping of the major FHB resistance gene Fhb7 derived from Thinopyrum ponticum and its pyramiding with Fhb1 by marker-assisted selection. . Theor. Appl. Genet. 128:(11):230116
    [Crossref] [Google Scholar]
  48. 48.
    Hafeez AN, Arora S, Ghosh S, Gilbert D, Bowden RL, Wulff BBH. 2021.. Creation and judicious application of a wheat resistance gene atlas. . Mol. Plant 14:(7):105370
    [Crossref] [Google Scholar]
  49. 49.
    Hafeez AN, Chartrain L, Feng C, Cambon F, Clarke M, et al. 2023.. Septoria tritici blotch resistance gene Stb15 encodes a lectin receptor-like kinase. . bioRxiv 557217. https://doi.org/10.1101/2023.09.11.557217
  50. 50.
    Hall BH. 2007.. Patents and patent policy. . Oxf. Rev. Econ. Policy 23:(4):56887
    [Crossref] [Google Scholar]
  51. 51.
    Hao Y, Rasheed A, Zhu Z, Wulff BBH, He Z. 2020.. Harnessing wheat Fhb1 for Fusarium resistance. . Trends Plant Sci. 25:(1):13
    [Crossref] [Google Scholar]
  52. 52.
    Harding KL, Aguayo VM, Webb P. 2018.. Hidden hunger in South Asia: a review of recent trends and persistent challenges. . Public Health Nutr. 21:(4):78595
    [Crossref] [Google Scholar]
  53. 53.
    Hayta S, Smedley MA, Clarke M, Forner M, Harwood WA. 2021.. An efficient Agrobacterium-mediated transformation protocol for hexaploid and tetraploid wheat. . Curr. Protoc. 1:(3):e58
    [Crossref] [Google Scholar]
  54. 54.
    Hayta S, Smedley MA, Demir SU, Blundell R, Hinchliffe A, et al. 2019.. An efficient and reproducible Agrobacterium-mediated transformation method for hexaploid wheat (Triticum aestivum L.). . Plant Methods 15:(1):121
    [Crossref] [Google Scholar]
  55. 55.
    He Z, Chen M, Ling B, Cao T, Wang C, et al. 2023.. Overexpression of the autophagy-related gene SiATG8a from foxtail millet (Setaria italica L.) in transgenic wheat confers tolerance to phosphorus starvation. . Plant Physiol. Biochem. 196::58086
    [Crossref] [Google Scholar]
  56. 56.
    Hewitt T, Zhang J, Huang L, Upadhyaya N, Li J, et al. 2021.. Wheat leaf rust resistance gene Lr13 is a specific Ne2 allele for hybrid necrosis. . Mol. Plant 14:(7):102528
    [Crossref] [Google Scholar]
  57. 57.
    Hossain MM. 2022.. Wheat blast: a review from a genetic and genomic perspective. . Front. Microbiol. 13::983243
    [Crossref] [Google Scholar]
  58. 58.
    Huang L, Brooks SA, Li W, Fellers JP, Trick HN, Gill BS. 2003.. Map-based cloning of leaf rust resistance gene Lr21 from the large and polyploid genome of bread wheat. . Genetics 164:(2):65564
    [Crossref] [Google Scholar]
  59. 59.
    Hutter H-P, Poteser M, Lemmerer K, Wallner P, Kundi M, et al. 2021.. Health symptoms related to pesticide use in farmers and laborers of ecological and conventional banana plantations in Ecuador. . Int. J. Environ. Res. Public Health 18:(3):1126
    [Crossref] [Google Scholar]
  60. 60.
    ISAAA. 2023.. GM Approval Database. ISAAA. https://www.isaaa.org/gmapprovaldatabase/
    [Google Scholar]
  61. 61.
    Ishida Y, Tsunashima M, Hiei Y, Komari T. 2015.. Wheat (Triticum aestivum L.) transformation using immature embryos. . In Agrobacterium Protocols, 1, 18998. Methods Mol. Biol. 1223 . New York:: Springer
    [Google Scholar]
  62. 62.
    Jensen C, Saunders DGO. 2023.. Magnaporthe oryzae pathotype Triticum (MoT) can act as a heterologous expression system for fungal effectors with high transcript abundance in wheat. . Sci. Rep. 13:(1):108
    [Crossref] [Google Scholar]
  63. 63.
    Jhu M-Y, Oldroyd GED. 2023.. Dancing to a different tune, can we switch from chemical to biological nitrogen fixation for sustainable food security?. PLOS Biol. 21:(3):e3001982
    [Crossref] [Google Scholar]
  64. 64.
    Jiang L, Li R, Han Z, Zhao X, Cao D, Ow DW. 2022.. Target lines for recombinase-mediated gene stacking in soybean. . Theor. Appl. Genet. 135:(4):116375
    [Crossref] [Google Scholar]
  65. 65.
    Johal GS, Briggs SP. 1992.. Reductase activity encoded by the HM1 disease resistance gene in maize. . Science 258:(5084):98587
    [Crossref] [Google Scholar]
  66. 66.
    Jones DA, Thomas CM, Hammond-Kosack KE, Balint-Kurti PJ, Jones JDG. 1994.. Isolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging. . Science 266:(5186):78993
    [Crossref] [Google Scholar]
  67. 67.
    Joshi AK, Crossa J, Arun B, Chand R, Trethowan R, et al. 2010.. Genotype × environment interaction for zinc and iron concentration of wheat grain in eastern Gangetic plains of India. . Field Crop. Res. 116:(3):26877
    [Crossref] [Google Scholar]
  68. 68.
    Joshi S, Choukimath A, Isenegger D, Panozzo J, Spangenberg G, Kant S. 2019.. Improved wheat growth and yield by delayed leaf senescence using developmentally regulated expression of a cytokinin biosynthesis gene. . Front. Plant Sci. 10::1285
    [Crossref] [Google Scholar]
  69. 69.
    Jupe F, Witek K, Verweij W, Śliwka J, Pritchard L, et al. 2013.. Resistance gene enrichment sequencing (RenSeq) enables reannotation of the NB-LRR gene family from sequenced plant genomes and rapid mapping of resistance loci in segregating populations. . Plant J. 76:(3):53044
    [Crossref] [Google Scholar]
  70. 70.
    Kanyuka K. 2022.. Effector-triggered immunity, methods and protocols. . Methods Mol. Biol. 2523::93112
    [Crossref] [Google Scholar]
  71. 71.
    Katzen F. 2007.. Gateway® recombinational cloning: a biological operating system. . Expert Opin. Drug Discov. 2:(4):57189
    [Crossref] [Google Scholar]
  72. 72.
    Kieckhefer RW, Gellner JL. 1992.. Yield losses in winter wheat caused by low-density cereal aphid populations. . Agron. J. 84:(2):18083
    [Crossref] [Google Scholar]
  73. 73.
    Kirkland LS, Pirtle EI, Umina PA. 2018.. Responses of the Russian wheat aphid (Diuraphis noxia) and bird cherry oat aphid (Rhopalosiphum padi) to insecticide seed treatments in wheat. . Crop Pasture Sci. 69:(10):96673
    [Crossref] [Google Scholar]
  74. 74.
    Kolodziej MC, Singla J, Sánchez-Martín J, Zbinden H, Šimková H, et al. 2021.. A membrane-bound ankyrin repeat protein confers race-specific leaf rust disease resistance in wheat. . Nat. Commun. 12:(1):956
    [Crossref] [Google Scholar]
  75. 75.
    Kou J, Tang Q, Zhang X. 2015.. Agricultural GMO safety administration in China. . J. Integr. Agric. 14:(11):215765
    [Crossref] [Google Scholar]
  76. 76.
    Kourelis J, van der Hoorn RAL. 2018.. Defended to the nines: 25 years of resistance gene cloning identifies nine mechanisms for R protein function. . Plant Cell 30:(2):28599
    [Crossref] [Google Scholar]
  77. 77.
    Kumar R, Singh V, Pawar SK, Singh PK, Kaur A, Sharma D. 2019.. Wheat Production in Changing Environments: Responses, Adaptation and Tolerance. Singapore:: Springer
    [Google Scholar]
  78. 78.
    Lagudah ES, Krattinger SG. 2019.. A new player contributing to durable Fusarium resistance. . Nat. Genet. 51:(7):107071
    [Crossref] [Google Scholar]
  79. 79.
    Lampropoulos A, Sutikovic Z, Wenzl C, Maegele I, Lohmann JU, Forner J. 2013.. GreenGate: a novel, versatile, and efficient cloning system for plant transgenesis. . PLOS ONE 8:(12):e83043
    [Crossref] [Google Scholar]
  80. 80.
    Lapitan NLV, Peng J, Sharma V. 2007.. A high-density map and PCR markers for Russian wheat aphid resistance gene Dn7 on chromosome 1RS/1BL. . Crop Sci. 47:(2):81118
    [Crossref] [Google Scholar]
  81. 81.
    Lerro CC, Freeman LEB, DellaValle CT, Andreotti G, Hofmann JN, et al. 2021.. Pesticide exposure and incident thyroid cancer among male pesticide applicators in agricultural health study. . Environ. Int. 146::106187
    [Crossref] [Google Scholar]
  82. 82.
    Lesk C, Rowhani P, Ramankutty N. 2016.. Influence of extreme weather disasters on global crop production. . Nature 529:(7584):8487
    [Crossref] [Google Scholar]
  83. 83.
    Li G, Zhou J, Jia H, Gao Z, Fan M, et al. 2019.. Mutation of a histidine-rich calcium-binding-protein gene in wheat confers resistance to Fusarium head blight. . Nat. Genet. 51:(7):110612
    [Crossref] [Google Scholar]
  84. 84.
    Li Y, Wei Z-Z, Sela H, Govta L, Klymiuk V, et al. 2022.. Long-read genome sequencing accelerated the cloning of Pm69 by resolving the complexity of a rapidly evolving resistance gene cluster in wheat. . bioRxiv 512294. https://doi.org/10.1101/2022.10.14.512294
  85. 85.
    Lin Q, Jin S, Zong Y, Yu H, Zhu Z, et al. 2021.. High-efficiency prime editing with optimized, paired pegRNAs in plants. . Nat. Biotechnol. 39:(8):92327
    [Crossref] [Google Scholar]
  86. 86.
    Lopez HW, Krespine V, Lemair A, Coudray C, Feillet-Coudray C, et al. 2003.. Wheat variety has a major influence on mineral bioavailability; studies in rats. . J. Cereal Sci. 37:(3):25766
    [Crossref] [Google Scholar]
  87. 87.
    Luo M, Xie L, Chakraborty S, Wang A, Matny O, et al. 2021.. A five-transgene cassette confers broad-spectrum resistance to a fungal rust pathogen in wheat. . Nat. Biotechnol. 39:(5):56166
    [Crossref] [Google Scholar]
  88. 88.
    Mao H, Li S, Chen B, Jian C, Mei F, et al. 2022.. Variation in cis-regulation of a NAC transcription factor contributes to drought tolerance in wheat. . Mol. Plant 15:(2):27692
    [Crossref] [Google Scholar]
  89. 89.
    Marchal C, Zhang J, Zhang P, Fenwick P, Steuernagel B, et al. 2018.. BED-domain-containing immune receptors confer diverse resistance spectra to yellow rust. . Nat. Plants 4:(9):66268
    [Crossref] [Google Scholar]
  90. 90.
    McDonald BA, Linde C. 2002.. Pathogen population genetics, evolutionary potential, and durable resistance. . Phytopathology 40:(1):34979
    [Crossref] [Google Scholar]
  91. 91.
    Minhas PS, Rane J, Pasala RK. 2017.. Abiotic Stress Management for Resilient Agriculture. Singapore:: Springer
    [Google Scholar]
  92. 92.
    Morran S, Eini O, Pyvovarenko T, Parent B, Singh R, et al. 2011.. Improvement of stress tolerance of wheat and barley by modulation of expression of DREB/CBF factors. . Plant Biotechnol. J. 9:(2):23049
    [Crossref] [Google Scholar]
  93. 93.
    Nancarrow N, Aftab M, Freeman A, Rodoni B, Hollaway G, Trębicki P. 2018.. Prevalence and incidence of yellow dwarf viruses across a climatic gradient: a four-year field study in southeastern Australia. . Plant Dis. 102:(12):246572
    [Crossref] [Google Scholar]
  94. 94.
    Nat. Biotechnol. 2021.. Argentina first to market with drought-resistant GM wheat. . Nat. Biotechnol. 39:(6):652
    [Crossref] [Google Scholar]
  95. 95.
    OECD. 2003.. Consensus document on compositional considerations for new varieties of bread wheat (Triticum aestivum): key food and feed nutrients, anti-nutrients and toxicants. Ser. Saf. Nov. Foods Feeds No. 7 , Organ. Econ. Co-op. Dev. (OECD), Paris:
    [Google Scholar]
  96. 96.
    Oerke E-C, Dehne H-W. 2004.. Safeguarding production—losses in major crops and the role of crop protection. . Crop Prot. 23:(4):27585
    [Crossref] [Google Scholar]
  97. 97.
    O'Hara T, Steed A, Goddard R, Gaurav K, Arora S, et al. 2023.. The wheat powdery mildew resistance gene Pm4 also confers resistance to wheat blast. . bioRxiv 559489. https://doi.org/10/1101/2023.09.26.559489
  98. 98.
    Ow DW. 2016.. The long road to recombinase-mediated plant transformation. . Plant Biotechnol. J. 14:(2):44147
    [Crossref] [Google Scholar]
  99. 99.
    Paine JA, Shipton CA, Chaggar S, Howells RM, Kennedy MJ, et al. 2005.. Improving the nutritional value of Golden Rice through increased pro-vitamin A content. . Nat. Biotechnol. 23:(4):48287
    [Crossref] [Google Scholar]
  100. 100.
    Pierre CS, Crossa JL, Bonnett D, Yamaguchi-Shinozaki K, Reynolds MP. 2012.. Phenotyping transgenic wheat for drought resistance. . J. Exp. Bot. 63:(5):1799808
    [Crossref] [Google Scholar]
  101. 101.
    Raman V, Rojas CM, Vasudevan B, Dunning K, Kolape J, et al. 2022.. Agrobacterium expressing a type III secretion system delivers Pseudomonas effectors into plant cells to enhance transformation. . Nat. Commun. 13:(1):2581
    [Crossref] [Google Scholar]
  102. 102.
    Rawat N, Pumphrey MO, Liu S, Zhang X, Tiwari VK, et al. 2016.. Wheat Fhb1 encodes a chimeric lectin with agglutinin domains and a pore-forming toxin-like domain conferring resistance to Fusarium head blight. . Nat. Genet. 48:(12):157680
    [Crossref] [Google Scholar]
  103. 103.
    Sanahuja G, Banakar R, Twyman RM, Capell T, Christou P. 2011.. Bacillus thuringiensis: a century of research, development and commercial applications. . Plant Biotechnol. J. 9:(3):283300
    [Crossref] [Google Scholar]
  104. 104.
    Sánchez-Martín J, Steuernagel B, Ghosh S, Herren G, Hurni S, et al. 2016.. Rapid gene isolation in barley and wheat by mutant chromosome sequencing. . Genome Biol. 17:(1):221
    [Crossref] [Google Scholar]
  105. 105.
    Sánchez-Martín J, Widrig V, Herren G, Wicker T, Zbinden H, et al. 2021.. Wheat Pm4 resistance to powdery mildew is controlled by alternative splice variants encoding chimeric proteins. . Nat. Plants 7:(3):32741
    [Crossref] [Google Scholar]
  106. 106.
    Santiago-González JC, Kerns DL, Head GP, Yang F. 2022.. Effective dominance and redundant killing of single- and dual-gene resistant populations of Helicoverpa zea on pyramided Bt corn and cotton. . Pest Manag. Sci. 78:(10):433339
    [Crossref] [Google Scholar]
  107. 107.
    Saripalli G, Adhikari L, Amos C, Kibriya A, Ahmed HI, et al. 2023.. Integration of genetic and genomics resources in einkorn wheat enables precision mapping of important traits. . Commun. Biol. 6:(1):835
    [Crossref] [Google Scholar]
  108. 108.
    Sarrion-Perdigones A, Falconi EE, Zandalinas SI, Juárez P, Fernández-del-Carmen A, et al. 2011.. GoldenBraid: an iterative cloning system for standardized assembly of reusable genetic modules. . PLOS ONE 6:(7):e21622
    [Crossref] [Google Scholar]
  109. 109.
    Saulnier L, Sado P-E, Branlard G, Charmet G, Guillon F. 2007.. Wheat arabinoxylans: Exploiting variation in amount and composition to develop enhanced varieties. . J. Cereal Sci. 46:(3):26181
    [Crossref] [Google Scholar]
  110. 110.
    Saur IML, Bauer S, Lu X, Schulze-Lefert P. 2019.. A cell death assay in barley and wheat protoplasts for identification and validation of matching pathogen AVR effector and plant NLR immune receptors. . Plant Methods 15:(1):118
    [Crossref] [Google Scholar]
  111. 111.
    Savary S, Willocquet L, Pethybridge SJ, Esker P, McRoberts N, Nelson A. 2019.. The global burden of pathogens and pests on major food crops. . Nat. Ecol. Evol. 3:(3):43039
    [Crossref] [Google Scholar]
  112. 112.
    Sharma D, Avni R, Gutierrez-Gonzalez J, Kumar R, Sela H, et al. 2023.. A single NLR gene confers resistance to leaf and stripe rust in wheat. . Res. Square. https://doi.org/10.21203/rs.3.rs-3146908/v1
  113. 113.
    Shewry PR, Charmet G, Branlard G, Lafiandra D, Gergely S, et al. 2012.. Developing new types of wheat with enhanced health benefits. . Trends Food Sci. Technol. 25:(2):7077
    [Crossref] [Google Scholar]
  114. 114.
    Sidhu GK, Singh S, Kumar V, Dhanjal DS, Datta S, Singh J. 2019.. Toxicity, monitoring and biodegradation of organophosphate pesticides: a review. . Crit. Rev. Environ. Sci. Technol. 49:(13):113587
    [Crossref] [Google Scholar]
  115. 115.
    Singh RP, Singh PK, Rutkoski J, Hodson DP, He X, et al. 2015.. Disease impact on wheat yield potential and prospects of genetic control. . Annu. Rev. Phytopathol. 54::30322
    [Crossref] [Google Scholar]
  116. 116.
    Singh SP, Keller B, Gruissem W, Bhullar NK. 2017.. Rice NICOTIANAMINE SYNTHASE 2 expression improves dietary iron and zinc levels in wheat. . Theor. Appl. Genet. 130:(2):28392
    [Crossref] [Google Scholar]
  117. 117.
    Smith CM. 2005.. Plant Resistance to Arthropods: Molecular and Conventional Approaches. Dordrecht, Neth:.: Springer
    [Google Scholar]
  118. 118.
    Steuernagel B, Periyannan SK, Hernández-Pinzón I, Witek K, Rouse MN, et al. 2016.. Rapid cloning of disease-resistance genes in plants using mutagenesis and sequence capture. . Nat. Biotechnol. 34:(6):65255
    [Crossref] [Google Scholar]
  119. 119.
    Su Z, Bernardo A, Tian B, Chen H, Wang S, et al. 2019.. A deletion mutation in TaHRC confers Fhb1 resistance to Fusarium head blight in wheat. . Nat. Genet. 51:(7):1099105
    [Crossref] [Google Scholar]
  120. 120.
    Sun C, Lei Y, Li B, Gao Q, Li Y, et al. 2024.. Precise integration of large DNA sequences in plant genomes using PrimeRoot editors. . Nat. Biotechnol. 42::31627
    [Crossref] [Google Scholar]
  121. 121.
    Tabashnik BE, Fabrick JA, Carrière Y. 2023.. Global patterns of insect resistance to transgenic Bt crops: the first 25 years. . J. Econ. Entomol. 116:(2):297309
    [Crossref] [Google Scholar]
  122. 122.
    Thind AK, Wicker T, Šimková H, Fossati D, Moullet O, et al. 2017.. Rapid cloning of genes in hexaploid wheat using cultivar-specific long-range chromosome assembly. . Nat. Biotechnol. 35:(8):79396
    [Crossref] [Google Scholar]
  123. 123.
    Tucker MA, Lopez-Ruiz F, Jayasena K, Oliver RP. 2015.. Origin of fungicide-resistant barley powdery mildew in western Australia: lessons to be learned. . In Fungicide Resistance in Plant Pathogens: Principles and a Guide to Practical Management, ed. H Ishii, DW Hollomon , pp. 32940. Tokyo:: Springer
    [Google Scholar]
  124. 124.
    UN. 1992.. Report of the United Nations Conference on Environment and Development. Rep. , United Nations, New York:. https://www.un.org/esa/dsd/agenda21/Agenda%2021.pdf
    [Google Scholar]
  125. 125.
    USPTO. 2023.. Manual of patent examining procedure, ninth edition, revision 07.2022. Rep. , USPTO, Alexandria, VA:. https://www.uspto.gov/web/offices/pac/mpep/index.html
    [Google Scholar]
  126. 126.
    Walkowiak S, Gao L, Monat C, Haberer G, Kassa MT, et al. 2020.. Multiple wheat genomes reveal global variation in modern breeding. . Nature 588:(7837):27783
    [Crossref] [Google Scholar]
  127. 127.
    Wang H, Sun S, Ge W, Zhao L, Hou B, et al. 2020.. Horizontal gene transfer of Fhb7 from fungus underlies Fusarium head blight resistance in wheat. . Science 368:(6493):eaba5435
    [Crossref] [Google Scholar]
  128. 128.
    Wani SH, Gaikwad K, Razzaq A, Samantara K, Kumar M, Govindan V. 2022.. Improving zinc and iron biofortification in wheat through genomics approaches. . Mol. Biol. Rep. 49:(8):800723
    [Crossref] [Google Scholar]
  129. 129.
    Webber PM. 2003.. Protecting your inventions: the patent system. . Nat. Rev. Drug Discov. 2:(10):82330
    [Crossref] [Google Scholar]
  130. 130.
    Weber E, Engler C, Gruetzner R, Werner S, Marillonnet S. 2011.. A modular cloning system for standardized assembly of multigene constructs. . PLOS ONE 6:(2):e16765
    [Crossref] [Google Scholar]
  131. 131.
    Wiese MV. 1987.. Compendium of Wheat Diseases. St. Paul, MN:: APS Press
    [Google Scholar]
  132. 132.
    Wulff BB, Dhugga KS. 2018.. Wheat—the cereal abandoned by GM. . Science 361:(6401):45152
    [Crossref] [Google Scholar]
  133. 133.
    Wulff BB, Krattinger SG. 2022.. The long road to engineering durable disease resistance in wheat. . Curr. Opin. Biotechnol. 73::27075
    [Crossref] [Google Scholar]
  134. 134.
    Xi J, Patel M, Dong S, Que Q, Qu R. 2018.. Acetosyringone treatment duration affects large T-DNA molecule transfer to rice callus. . BMC Biotechnol. 18:(1):48
    [Crossref] [Google Scholar]
  135. 135.
    Xing L, Hu P, Liu J, Witek K, Zhou S, et al. 2018.. Pm21 from Haynaldia villosa encodes a CC-NBS-LRR protein conferring powdery mildew resistance in wheat. . Mol. Plant 11:(6):87478
    [Crossref] [Google Scholar]
  136. 136.
    Yan X, Li M, Zhang P, Yin G, Zhang H, et al. 2021.. High-temperature wheat leaf rust resistance gene Lr13 exhibits pleiotropic effects on hybrid necrosis. . Mol. Plant 14:(7):102932
    [Crossref] [Google Scholar]
  137. 137.
    Yang Y, Luang S, Harris J, Riboni M, Li Y, et al. 2018.. Overexpression of the class I homeodomain transcription factor TaHDZipI-5 increases drought and frost tolerance in transgenic wheat. . Plant Biotechnol. J. 16:(6):122740
    [Crossref] [Google Scholar]
  138. 138.
    Yu G, Matny O, Champouret N, Steuernagel B, Moscou MJ, et al. 2022.. Aegilops sharonensis genome-assisted identification of stem rust resistance gene Sr62. . Nat. Commun. 13:(1):1607
    [Crossref] [Google Scholar]
  139. 139.
    Yu T-F, Xu Z-S, Guo J-K, Wang Y-X, Abernathy B, et al. 2017.. Improved drought tolerance in wheat plants overexpressing a synthetic bacterial cold shock protein gene. . Sci. Rep. 7:(1):44050
    [Crossref] [Google Scholar]
  140. 140.
    Zetterberg C, Björnberg KE. 2017.. Time for a new EU regulatory framework for GM crops?. J. Agric. Environ. Ethics 30:(3):32547
    [Crossref] [Google Scholar]
  141. 141.
    Zhang H, Zhu J, Gong Z, Zhu J-K. 2022.. Abiotic stress responses in plants. . Nat. Rev. Genet. 23:(2):10419
    [Crossref] [Google Scholar]
  142. 142.
    Zhang J, Hewitt TC, Boshoff WHP, Dundas I, Upadhyaya N, et al. 2021.. A recombined Sr26 and Sr61 disease resistance gene stack in wheat encodes unrelated NLR genes. . Nat. Commun. 12:(1):3378
    [Crossref] [Google Scholar]
  143. 143.
    Zhang J, Nirmala J, Chen S, Jost M, Steuernagel B, et al. 2023.. Single amino acid change alters specificity of the multi-allelic wheat stem rust resistance locus SR9. . Nat. Commun. 14:(1):7354
    [Crossref] [Google Scholar]
/content/journals/10.1146/annurev-phyto-121423-042128
Loading
/content/journals/10.1146/annurev-phyto-121423-042128
Loading

Data & Media loading...

Supplemental Materials

Supplemental Materials

Supplemental Materials

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error