Modification of cereal plant architecture by genome editing to improve yields

Abstract

Key Message

We summarize recent genome editing studies that have focused on the examination (or reexamination) of plant architectural phenotypes in cereals and the modification of these traits for crop improvement.

Abstract

Plant architecture is defined as the three-dimensional organization of the entire plant. Shoot architecture refers to the structure and organization of the aboveground components of a plant, reflecting the developmental patterning of stems, branches, leaves and inflorescences/flowers. Root system architecture is essentially determined by four major shape parameters—growth, branching, surface area and angle. Interest in plant architecture has arisen from the profound impact of many architectural traits on agronomic performance, and the genetic and hormonal regulation of these traits which makes them sensitive to both selective breeding and agronomic practices. This is particularly important in staple crops, and a large body of literature has, therefore, accumulated on the control of architectural phenotypes in cereals, particularly rice due to its twin role as one of the world’s most important food crops as well as a model organism in plant biology and biotechnology. These studies have revealed many of the molecular mechanisms involved in the regulation of tiller/axillary branching, stem height, leaf and flower development, root architecture and the grain characteristics that ultimately help to determine yield. The advent of genome editing has made it possible, for the first time, to introduce precise mutations into cereal crops to optimize their architecture and close in on the concept of the ideotype. In this review, we consider recent genome editing studies that have focused on the examination (or reexamination) of plant architectural phenotypes in cereals and the modification of these traits for crop improvement.

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References

  1. Ai H, Cao Y, Jain A, Wang X, Hu Z, Zhao G, Hu S, Shen X, Yan Y, Liu X, Sun Y, Lan X, Xu G, Sun S (2020) The ferroxidase LPR5 functions in the maintenance of phosphate homeostasis and is required for normal growth and development of rice. J Exp Bot 71:4828–4842

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  2. Alqudah AM, Schnurbusch T (2017) Heading date is not flowering time in spring barley. Front Plant Sci 8:896. https://doi.org/10.3389/fpls.2017.00896

    Article  PubMed  PubMed Central  Google Scholar 

  3. Armario Najera V, Twyman RM, Christou P, Zhu C (2019) Applications of multiplex genome editing in higher plants. Curr Opin Biotechnol 59:93–102

    CAS  PubMed  Article  Google Scholar 

  4. Ashikari M, Sakakibara H, Lin S, Yamamoto T, Takashi T, Nishimura A, Angeles ER, Qian Q, Kitano H, Matsuoka M (2005) Cytokinin oxidase regulates rice grain production. Science 309:741–745

    CAS  PubMed  Article  Google Scholar 

  5. Biswas S, Tian J, Li R, Chen X, Luo Z, Chen M, Zhao X, Zhang D, Persson S, Yuan Z, Shi J (2020) Investigation of CRISPR/Cas9-induced SD1 rice mutants highlights the importance of molecular characterization in plant molecular breeding. J Genet Genomics 47:273–280

    PubMed  Article  Google Scholar 

  6. Burr CA, Sun J, Yamburenko MV, Willoughby A, Hodgens C, Boeshore SL, Elmore A, Atkinson J, Nimchuk ZL, Bishopp A, Schaller GE, Kieber JJ (2020) The HK5 and HK6 cytokinin receptors mediate diverse developmental pathways in rice. Development 147:dev191734. https://doi.org/10.1242/dev.191734

    Article  PubMed  Google Scholar 

  7. Butt H, Jamil M, Wang JY, Al-Babili S, Mahfouz M (2018) Engineering plant architecture via CRISPR/Cas9-mediated alteration of strigolactone biosynthesis. BMC Plant Biol 18:174. https://doi.org/10.1186/s12870-018-1387-1

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  8. Chen Y, Dan Z, Gao F, Chen P, Fan F, Li S (2020) Rice GROWTH-REGULATING FACTOR7 modulates plant architecture through regulating GA and IAA metabolism. Plant Physiol 184:393–406

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  9. Chiou WY, Kawamoto T, Himi E, Rikiishi K, Sugimoto M, Hayashi-Tsugane M, Tsugane K, Maekawa M (2019) LARGE GRAIN encodes a putative RNA-binding protein that regulates spikelet hull length in rice. Plant Cell Physiol 60:503–515

    CAS  PubMed  Article  Google Scholar 

  10. Cong B, Tanksley SD (2006) FW2.2 and cell cycle control in developing tomato fruit: a possible example of gene co-option in the evolution of a novel organ. Plant Mol Biol 62:867–880

    CAS  PubMed  Article  Google Scholar 

  11. Coudert Y, Perin C, Courtois B, Khong NG, Gantet P (2010) Genetic control of root development in rice, the model cereal. Trends Plant Sci 15:219–226

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  12. Cui Y, Zhu M, Xu Z, Xu Q (2019) Assessment of the effect of ten heading time genes on reproductive transition and yield components in rice using a CRISPR/Cas9 system. Theor Appl Genet 132:1887–1896

    CAS  PubMed  Article  Google Scholar 

  13. Cui Y, Jiang N, Xu Z, Xu Q (2020a) Heterotrimeric G protein are involved in the regulation of multiple agronomic traits and stress tolerance in rice. BMC Plant Biol 20:90. https://doi.org/10.1186/s12870-020-2289-6

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  14. Cui Y, Hu X, Liang G, Feng A, Wang F, Ruan S, Dong G, Shen L, Zhang B, Chen D, Zhu L, Hu J, Lin Y, Guo L, Matsuoka M, Qian Q (2020b) Production of novel beneficial alleles of a rice yield-related QTL by CRISPR/Cas9. Plant Biotechnol J 18:1987–1989

    CAS  PubMed Central  Article  PubMed  Google Scholar 

  15. Dai M, Zhao Y, Ma Q, Hu Y, Hedden P, Zhang Q, Zhou DX (2007) The rice YABBY1 gene is involved in the feedback regulation of gibberellin metabolism. Plant Physiol 144:121–133

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  16. Deng X, Han X, Yu S, Liu Z, Guo D, He Y, Li W, Tao Y, Sun C, Xu P, Liao Y, Chen X, Zhang H, Wu X (2020) OsINV3 and its homolog, OsINV2, control grain size in rice. Int J Mol Sci 21:2199. https://doi.org/10.3390/ijms21062199

    CAS  Article  PubMed Central  PubMed  Google Scholar 

  17. Dkhar J, Pareek A (2014) What determines a leaf’s shape? Evodevo 5:47. https://doi.org/10.1186/2041-9139-5-47

    Article  PubMed  PubMed Central  Google Scholar 

  18. Doebley J, Stec A, Gustus C (1995) teosinte branched1 and the origin of maize: evidence for epistasis and the evolution of dominance. Genetics 141:333–346

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  19. Donald CM (1968) Breeding of crop ideotypes. Euphytica 17:385–403

    Article  Google Scholar 

  20. Duan J, Yu H, Yuan K, Liao Z, Meng X, Jing Y, Liu G, Chu J, Li J (2019) Strigolactone promotes cytokinin degradation through transcriptional activation of CYTOKININ OXIDASE/DEHYDROGENASE 9 in rice. Proc Natl Acad Sci USA 116:14319–14324

    CAS  PubMed  Article  Google Scholar 

  21. Fan C, Xing Y, Mao H, Lu T, Han B, Xu C, Li X, Zhang Q (2006) GS3, a major QTL for grain length and weight and minor QTL for grain width and thickness in rice, encodes a putative transmembrane protein. Theor Appl Genet 112:1164–1171

    CAS  PubMed  Article  Google Scholar 

  22. Gao Q, Li G, Sun H, Xu M, Wang H, Ji J, Wang D, Yuan C, Zhao X (2020) Targeted mutagenesis of the rice FW2.2-like gene family using the CRISPR/Cas9 system reveals OsFWL4 as a regulator of tiller number and plant yield in rice. Int J Mol Sci 21:809. https://doi.org/10.3390/ijms21030809

    CAS  Article  PubMed Central  PubMed  Google Scholar 

  23. Gasparis S, Przyborowski M, Kala M, Nadolska-Orczyk A (2019) Knockout of the HvCKX1 or HvCKX3 gene in barley (Hordeum vulgare L.) by RNA-guided Cas9 nuclease affects the regulation of cytokinin metabolism and toot morphology. Cells 8:782. https://doi.org/10.3390/cells8080782

    CAS  Article  PubMed Central  PubMed  Google Scholar 

  24. Guo M, Rupe MA, Wei J, Winkler C, Goncalves-Butruille M, Weers BP, Cerwick SF, Dieter JA, Duncan KE, Howard RJ, Hou Z, Loffler CM, Cooper M, Simmons CR (2014) Maize ARGOS1 (ZAR1) transgenic alleles increase hybrid maize yield. J Exp Bot 65:249–260

    CAS  PubMed  Article  Google Scholar 

  25. Guo T, Lu Z, Shan J, Ye W, Dong N, Lin H (2020) ERECTA1 acts upstream of the OsMKKK10-OsMKK4-OsMPK6 cascade to control spikelet number by regulating cytokinin metabolism in rice. Plant Cell 2:2763–2779

    Article  CAS  Google Scholar 

  26. Han Y, Teng K, Nawaz G, Feng X, Usman B, Wang X, Luo L, Zhao N, Liu Y, Li R (2019) Generation of semi-dwarf rice (Oryza sativa L.) lines by CRISPR/Cas9-directed mutagenesis of OsGA20ox2 and proteomic analysis of unveiled changes caused by mutations. Biotech 9:387. https://doi.org/10.1007/s13205-019-1919-x

    Article  Google Scholar 

  27. Hu X, Cui Y, Dong G, Feng A, Wang D, Zhao C, Zhang Y, Hu J, Zeng D, Guo L, Qian Q (2019) Using CRISPR-Cas9 to generate semi-dwarf rice lines in elite landraces. Sci Rep 9:19096. https://doi.org/10.1038/s41598-019-55757-9

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  28. Hu L, Tu B, Yang W, Yuan H, Li J, Guo L, Zheng L, Chen W, Zhu X, Wang Y, Qin P, Ma B, Li S (2020a) Mitochondria-associated pyruvate kinase complexes regulate grain filling in rice. Plant Physiol 183:1073–1087

    CAS  PubMed  Article  Google Scholar 

  29. Hu Y, Li S, Fan X, Song S, Zhou X, Weng X, Xiao J, Li X, Xiong L, You A, Xing Y (2020b) OsHOX1 and OsHOX28 redundantly shape rice tiller angle by reducing HSFA2D expression and auxin content. Plant Physiol 184:1424–1437

    CAS  PubMed  Article  Google Scholar 

  30. Huang X, Qian Q, Liu Z, Sun H, He S, Luo D, Xia G, Chu C, Li J, Fu X (2009) Natural variation at the DEP1 locus enhances grain yield in rice. Nat Genet 41:494–497

    CAS  PubMed  Article  Google Scholar 

  31. Huang J, Li J, Zhou J, Wang L, Yang S, Hurst LD, Li WH, Tian D (2018) Identifying a large number of high-yield genes in rice by pedigree analysis, whole-genome sequencing, and CRISPR-Cas9 gene knockout. Proc Natl Acad Sci USA 115:E7559–E7567

    CAS  PubMed  Article  Google Scholar 

  32. Huang Y, Bai X, Luo M, Xing Y (2019) Short Panicle 3 controls panicle architecture by upregulating APO2/RFL and increasing cytokinin content in rice. J Integr Plant Biol 61:987–999

    CAS  PubMed  Article  Google Scholar 

  33. Ji X, Du Y, Li F, Sun H, Zhang J, Li J, Peng T, Xin Z, Zhao Q (2019) The basic helix-loop-helix transcription factor, OsPIL15, regulates grain size via directly targeting a purine permease gene OsPUP7 in rice. Plant Biotechnol J 17:1527–1537

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  34. Ji Y, Huang W, Wu B, Fang Z, Wang X (2020) The amino acid transporter AAP1 mediates growth and grain yield by regulating neutral amino acid uptake and reallocation in Oryza sativa. J Exp Bot 71:4763–4777

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  35. Jia S, Xiong Y, Xiao P, Wang X, Yao J (2019) OsNF-YC10, a seed preferentially expressed gene regulates grain width by affecting cell proliferation in rice. Plant Sci 280:219–227

    CAS  PubMed  Article  Google Scholar 

  36. Jiao Y, Wang Y, Xue D, Wang J, Yan M, Liu G, Dong G, Zeng D, Lu Z, Zhu X, Qian Q, Li J (2010) Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat Genet 42:541–544

    CAS  PubMed  Article  Google Scholar 

  37. Johnston R, Wang M, Sun Q, Sylvester AW, Hake S, Scanlon MJ (2014) Transcriptomic analyses indicate that maize ligule development recapitulates gene expression patterns that occur during lateral organ initiation. Plant Cell 26:4718–4732

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  38. Juarez MT, Kui S, Thomas J, Heller BA, Timmermans MC (2004a) MicroRNA-mediated repression of rolled leaf1 specifies maize leaf polarity. Nature 428:84–88

    CAS  PubMed  Article  Google Scholar 

  39. Juarez MT, Twigg RW, Timmermans MC (2004b) Specification of adaxial cell fate during maize leaf development. Development 131:4533–4544

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  40. Khush GS (2001) Green revolution: the way forward. Nat Rev Genet 2:815–822

    CAS  PubMed  Article  Google Scholar 

  41. Kitomi Y, Hanzawa E, Kuya N, Inoue H, Hara N, Kawai S, Kanno N, Endo M, Sugimoto K, Yamazaki T, Sakamoto S, Sentoku N, Wu J, Kanno H, Mitsuda N, Toriyama K, Sato T, Uga Y (2020) Root angle modifications by the DRO1 homolog improve rice yields in saline paddy fields. Proc Natl Acad Sci USA 117:21242–21250

    CAS  PubMed  Article  Google Scholar 

  42. Konishi S, Izawa T, Lin SY, Ebana K, Fukuta Y, Sasaki T, Yano M (2006) An SNP caused loss of seed shattering during rice domestication. Science 312:1392–1396

    CAS  PubMed  Article  Google Scholar 

  43. Krecek P, Skupa P, Libus J, Naramoto S, Tejos R, Friml J, Zazímalova E (2009) The PIN-FORMED (PIN) protein family of auxin transporters. Genome Biol 10:249. https://doi.org/10.1186/gb-2009-10-12-249

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  44. Lee DW, Lee SK, Rahman MM, Kim YJ, Zhang D, Jeon JS (2019a) The role of rice vacuolar invertase2 in seed size control. Mol Cells 42:711–720

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Lee HY, Chen Z, Zhang C, Yoon GM (2019b) Editing of the OsACS locus alters phosphate deficiency-induced adaptive responses in rice seedlings. J Exp Bot 70:1927–1940

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  46. Li N, Li Y (2016) Signaling pathways of seed size control in plants. Curr Opin Plant Biol 33:23–32

    PubMed  Article  CAS  Google Scholar 

  47. Li X, Qian Q, Fu Z, Wang Y, Xiong G, Zeng D, Wang X, Liu X, Teng S, Hiroshi F, Yuan M, Luo D, Han B, Li J (2003) Control of tillering in rice. Nature 422:618–621

    CAS  PubMed  Article  Google Scholar 

  48. Li M, Li X, Zhou Z, Wu P, Fang M, Pan X, Lin Q, Luo W, Wu G, Li H (2016a) Reassessment of the four yield-related genes Gn1a, DEP1, GS3, and IPA1 in rice using a CRISPR/Cas9 system. Front Plant Sci 7:377. https://doi.org/10.3389/fpls.2016.00377

    Article  PubMed  PubMed Central  Google Scholar 

  49. Li S, Gao F, Xie K, Zeng X, Cao Y, Zeng J, He Z, Ren Y, Li W, Deng Q, Wang S, Zheng A, Zhu J, Liu H, Wang L, Li P (2016b) The OsmiR396c-OsGRF4-OsGIF1 regulatory module determines grain size and yield in rice. Plant Biotechnol J 14:2134–2146

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  50. Li C, Liu C, Qi X, Wu Y, Fei X, Mao L, Cheng B, Li X, Xie C (2017a) RNA-guided Cas9 as an in vivo desired-target mutator in maize. Plant Biotechnol J 15:1566–1576

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  51. Li X, Zhou W, Ren Y, Tian X, Lv T, Wang Z, Fang J, Chu C, Yang J, Bu Q (2017b) High-efficiency breeding of early-maturing rice cultivars via CRISPR/Cas9-mediated genome editing. J Genet Genomics 44:175–178

    PubMed  Article  PubMed Central  Google Scholar 

  52. Li X, Tao Q, Miao J, Yang Z, Gu M, Liang G, Zhou Y (2019a) Evaluation of differential qPE9-1/DEP1 protein domains in rice grain length and weight variation. Rice (N Y) 12:5. https://doi.org/10.1186/s12284-019-0263-4

    Article  Google Scholar 

  53. Li Y, Zhu J, Wu L, Shao Y, Wu Y, Mao C (2019b) Functional divergence of PIN1 paralogous genes in rice. Plant Cell Physiol 60:2720–2732

    CAS  PubMed  Article  Google Scholar 

  54. Liao S, Qin X, Luo L, Han Y, Wang X, Usman B, Nawaz G, Zhao N, Liu Y, Li R (2019) CRISPR/Cas9-induced mutagenesis of semi-rolled leaf1, 2 confers curled leaf phenotype and drought tolerance by influencing protein expression patterns and ROS scavenging in rice (Oryza sativa L.). Agronomy 9:728. https://doi.org/10.3390/agronomy9110728

    CAS  Article  Google Scholar 

  55. Lin Q, Zhang Z, Wu F, Feng M, Sun Y, Chen W, Cheng Z, Zhang X, Ren Y, Lei C, Zhu S, Wang J, Zhao Z, Guo X, Wang H, Wan J (2020) The APC/CTE E3 ubiquitin ligase complex mediates the antagonistic regulation of root growth and tillering by ABA and GA. Plant Cell 32:1973–1987

    CAS  PubMed  Article  Google Scholar 

  56. Liu J, Chen J, Zheng X, Wu F, Lin Q, Heng Y, Tian P, Cheng Z, Yu X, Zhou K, Zhang X, Guo X, Wang J, Wang H, Wan J (2017) GW5 acts in the brassinosteroid signalling pathway to regulate grain width and weight in rice. Nat Plants 3:17043. https://doi.org/10.1038/nplants.2017.43

    CAS  Article  PubMed  Google Scholar 

  57. Liu E, Zeng S, Zhu S, Liu Y, Wu G, Zhao K, Liu X, Liu Q, Dong Z, Dang X, Xie H, Li D, Hu X, Hong D (2019) Favorable alleles of GRAIN-FILLING RATE1 increase the grain-filling rate and yield of rice. Plant Physiol 181:1207–1222

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  58. Lu K, Wu B, Wang J, Zhu W, Nie H, Qian J, Huang W, Fang Z (2018) Blocking amino acid transporter OsAAP3 improves grain yield by promoting outgrowth buds and increasing tiller number in rice. Plant Biotechnol J 16:1710–1722

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  59. Ma L, Zhang D, Miao Q, Yang J, Xuan Y, Hu Y (2017) Essential role of sugar transporter OsSWEET11 during the early stage of rice grain filling. Plant Cell Physiol 58:863–873

    CAS  PubMed  Article  Google Scholar 

  60. Ma X, Feng F, Zhang Y, Elesawi IE, Xu K, Li T, Mei H, Liu H, Gao N, Chen C, Luo L, Yu S (2019) A novel rice grain size gene OsSNB was identified by genome-wide association study in natural population. PLoS Genet 15:e1008191. https://doi.org/10.1371/journal.pgen.1008191

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  61. Malcomber ST, Preston JC, Reinheimer R, Kossuth J, Kellogg EA (2006) Developmental gene evolution and the origin of grass inflorescence diversity. Adv Bot Res 44:425–481

    CAS  Article  Google Scholar 

  62. Mao C, He J, Liu L, Deng Q, Yao X, Liu C, Qiao Y, Li P, Ming F (2020) OsNAC2 integrates auxin and cytokinin pathways to modulate rice root development. Plant Biotechnol J 18:429–442

    CAS  PubMed  Article  Google Scholar 

  63. Miao J, Yang Z, Zhang D, Wang Y, Xu M, Zhou L, Wang J, Wu S, Yao Y, Du X, Gu F, Gong Z, Gu M, Liang G, Zhou Y (2019) Mutation of RGG2, which encodes a type B heterotrimeric G protein γ subunit, increases grain size and yield production in rice. Plant Biotechnol J 17:650–664

    CAS  PubMed  Article  Google Scholar 

  64. Minakuchi K, Kameoka H, Yasuno N, Umehara M, Luo L, Kobayashi K, Hanada A, Ueno K, Asami T, Yamaguchi S, Kyozuka J (2010) FINE CULM1 (FC1) works downstream of strigolactones to inhibit the outgrowth of axillary buds in rice. Plant Cell Physiol 51:1127–1135

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  65. Miura K, Ikeda M, Matsubara A, Song XJ, Ito M, Asano K, Matsuoka M, Kitano H, Ashikari M (2010) OsSPL14 promotes panicle branching and higher grain productivity in rice. Nat Genet 42:545–549

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  66. Morris EC, Griffiths M, Golebiowska A, Mairhofer S, Burr-Hersey J, Goh T, von Wangenheim D, Atkinson B, Sturrock CJ, Lynch JP, Vissenberg K, Ritz K, Wells DM, Mooney SJ, Bennett MJ (2017) Shaping 3D root system architecture. Curr Biol 27:R919–R930

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  67. Peng S, Laza RC, Visperas RM, Sanico AL, Cassman KL, Khush GS (2000) Grain yield of rice cultivars and lines developed in Philippines since 1996. Crop Sci 40:307–314

    Article  Google Scholar 

  68. Qian W, Wu C, Fu Y, Hu G, He Z, Liu W (2017) Novel rice mutants overexpressing the brassinosteroid catabolic gene CYP734A4. Plant Mol Biol 93:197–208

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  69. Qiao F, Yang Q, Wang C, Fan Y, Wu X, Zhao K (2007) Modification of plant height via RNAi suppression of OsGA20ox2 gene in rice. Euphytica 158:35–45

    CAS  Article  Google Scholar 

  70. Reinhardt D, Kuhlemeier C (2002) Plant architecture. EMBO Rep 3:846–851

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  71. Ren D, Hu J, Xu Q, Cui Y, Zhang Y, Zhou T, Rao Y, Xue D, Zeng D, Zhang G, Gao Z, Zhu L, Shen L, Chen G, Guo L, Qian Q (2018a) FZP determines grain size and sterile lemma fate in rice. J Exp Bot 69:4853–4866

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  72. Ren D, Yu H, Rao Y, Xu Q, Zhou T, Hu J, Zhang Y, Zhang G, Zhu L, Gao Z, Chen G, Guo L, Zeng D, Qian Q (2018b) ‘Two-floret spikelet’ as a novel resource has the potential to increase rice yield. Plant Biotechnol J 16:351–353

    PubMed  Article  Google Scholar 

  73. Ren D, Xu QK, Qiu ZN, Cui YJ, Zhou TT, Zeng DL, Guo LB, Qian Q (2019) FON4 prevents the multi-floret spikelet in rice. Plant Biotechnol J 17:1007–1009

    PubMed  PubMed Central  Article  Google Scholar 

  74. Ren D, Rao Y, Yu H, Xu Q, Cui Y, Xia S, Yu X, Liu H, Hu H, Xue D, Zeng D, Hu J, Zhang G, Gao Z, Zhu L, Zhang Q, Shen L, Guo L, Qian Q (2020) MORE FLORET1 encodes a MYB transcription factor that regulates spikelet development in rice. Plant Physiol 184:251–265

    CAS  PubMed  Article  Google Scholar 

  75. Rodriguez-Leal D, Lemmon ZH, Man J, Bartlett ME, Lippman ZB (2017) Engineering quantitative trait variation for crop improvement by genome editing. Cell 171:470–480

    CAS  PubMed  Article  Google Scholar 

  76. Ruan W, Guo M, Xu L, Wang X, Zhao H, Wang J, Yi K (2018) An SPX-RLI1 module regulates leaf inclination in response to phosphate availability in rice. Plant Cell 30:853–870

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  77. Sakamoto T, Kobayashi M, Itoh H, Tagiri A, Kayano T, Tanaka H, Iwahori S, Matsuoka M (2001) Expression of a gibberellin 2-oxidase gene around the shoot apex is related to phase transition in rice. Plant Physiol 125:1508–1516

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  78. Sakamoto T, Morinaka Y, Ishiyama K, Kobayashi M, Itoh H, Kayano T, Iwahori S, Matsuoka M, Tanaka H (2003) Genetic manipulation of gibberellin metabolism in transgenic rice. Nat Biotechnol 21:909–913

    CAS  PubMed  Article  Google Scholar 

  79. Santosh Kumar VV, Verma RK, Yadav SK, Yadav P, Watts A, Rao MV, Chinnusamy V (2020) CRISPR-Cas9 mediated genome editing of drought and salt tolerance (OsDST) gene in indica mega rice cultivar MTU1010. Physiol Mol Biol Plants 26:1099–1110

    CAS  PubMed  Article  Google Scholar 

  80. Shen L, Wang C, Fu Y, Wang J, Liu Q, Zhang X, Yan C, Qian Q, Wang (2018) QTL editing confers opposing yield performance in different rice varieties. J Integr Plant Biol 60:89–93

    CAS  PubMed  Article  Google Scholar 

  81. Sheng X, Sun Z, Wang X, Tan Y, Yu D, Yuan G, Yuan D, Duan M (2020) Improvement of the rice “Easy-to-Shatter” trait via CRISPR/Cas9-mediated mutagenesis of the qSH1 gene. Front Plant Sci 11:619. https://doi.org/10.3389/fpls.2020.00619

    Article  PubMed  PubMed Central  Google Scholar 

  82. Shi J, Habben JE, Archibald RL, Drummond BJ, Chamberlin MA, Williams RW, Lafitte HR, Weers BP (2015) Overexpression of ARGOS genes modifies plant sensitivity to ethylene, leading to improved drought tolerance in both Arabidopsis and maize. Plant Physiol 169:266–282

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  83. Shi J, Gao H, Wang H, Lafitte HR, Archibald RL, Yang M, Hakimi SM, Mo H, Habben JE (2017) ARGOS8 variants generated by CRISPR-Cas9 improve maize grain yield under field drought stress conditions. Plant Biotechnol J 15:207–216

    CAS  PubMed  Article  Google Scholar 

  84. Sinclair TR, Sheehy JE (1999) Erect leaves and photosynthesis in rice. Science 283:1455. https://doi.org/10.1126/science.283.5407.1455c

    Article  Google Scholar 

  85. Song XJ, Huang W, Shi M, Zhu MZ, Lin HX (2007) A QTL for rice grain width and weight encodes a previously unknown RING-type E3 ubiquitin ligase. Nat Genet 39:623–630

    CAS  PubMed  Article  Google Scholar 

  86. Strable J, Wallace JG, Unger-Wallace E, Briggs S, Bradbury PJ, Buckler ES, Vollbrecht E (2017) Maize YABBY genes drooping leaf1 and drooping leaf2 regulate plant architecture. Plant Cell 29:1622–1641

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  87. Sun S, Wang L, Mao H, Shao L, Li X, Xiao J, Ouyang Y, Zhang Q (2018) A G-protein pathway determines grain size in rice. Nat Commun 9:851. https://doi.org/10.1038/s41467-018-03141-y

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  88. Svitashev S, Schwartz C, Lenderts B, Young JK, Mark Cigan A (2016) Genome editing in maize directed by CRISPR-Cas9 ribonucleoprotein complexes. Nat Commun 7:13274. https://doi.org/10.1038/ncomms13274

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  89. Tian J, Wang C, Xia J, Wu L, Xu G, Wu W, Li D, Qin W, Han X, Chen Q, Jin W, Tian F (2019) Teosinte ligule allele narrows plant architecture and enhances high density maize yields. Science 365:658–664

    CAS  PubMed  Article  Google Scholar 

  90. Usman B, Nawaz G, Zhao N, Liu Y, Li R (2020) Generation of high yielding and fragrant rice (Oryza sativa L.) lines by CRISPR/Cas9 targeted mutagenesis of three homoeologs of cytochrome P450 gene family and OsBADH2 and transcriptome and proteome profiling of revealed changes triggered by mutations. Plants (Basel) 9:788. https://doi.org/10.3390/plants9060788

    CAS  Article  Google Scholar 

  91. Wang Y, Li J (2011) Branching in rice. Curr Opin Plant Biol 14:94–99

    CAS  PubMed  Article  Google Scholar 

  92. Wang Y, Geng L, Yuan M, Wei J, Jin C, Li M, Yu K, Zhang Y, Jin H, Wang E, Chai Z, Fu X, Li X (2017) Deletion of a target gene in Indica rice via CRISPR/Cas9. Plant Cell Rep 36:1333–1343

    CAS  PubMed  Article  Google Scholar 

  93. Wang B, Smith SM, Li J (2018a) Genetic regulation of shoot architecture. Ann Rev Plant Biol 69:437–468

    CAS  Article  Google Scholar 

  94. Wang W, Pan Q, He F, Akhunova A, Chao S, Trick H, Akhunov E (2018b) Transgenerational CRISPR-Cas9 activity facilitates multiplex gene editing in allopolyploid wheat. CRISPR J 1:65–74

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  95. Wang W, Simmonds J, Pan Q, Davidson D, He F, Battal A, Akhunova A, Trick HN, Uauy C, Akhunov E (2018c) Gene editing and mutagenesis reveal inter-cultivar differences and additivity in the contribution of TaGW2 homoeologues to grain size and weight in wheat. Theor Appl Genet 131:2463–2475

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  96. Wang B, Zhu L, Zhao B, Zhao Y, Xie Y, Zheng Z, Li Y, Sun J, Wang H (2019a) Development of a haploid-inducer mediated genome editing system for accelerating maize breeding. Mol Plant 12:597–602

    PubMed  Article  CAS  Google Scholar 

  97. Wang J, Wu B, Lu K, Wei Q, Qian J, Chen Y, Fang Z (2019b) The amino acid permease 5 (OsAAP5) regulates tiller number and grain yield in rice. Plant Physiol 180:1031–1045

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  98. Wang W, Pan Q, Tian B, He F, Chen Y, Bai G, Akhunova A, Trick HN, Akhunov E (2019c) Gene editing of the wheat homologs of TONNEAU1-recruiting motif encoding gene affects grain shape and weight in wheat. Plant J 100:251–264

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  99. Wang F, Han T, Song Q, Ye W, Song X, Chu J, Li J, Chen ZJ (2020a) Rice circadian clock regulates tiller growth and panicle development through strigolactone signaling and sugar sensing. Plant Cell. https://doi.org/10.1105/tpc.20.00289

    Article  PubMed  PubMed Central  Google Scholar 

  100. Wang G, Wang C, Lu G, Wang W, Mao G, Habben JE, Song C, Wang J, Chen J, Gao Y, Liu J, Greene TW (2020b) Knockouts of a late flowering gene via CRISPR-Cas9 confer early maturity in rice at multiple field locations. Plant Mol Biol 104:137–150

    CAS  PubMed  Article  Google Scholar 

  101. Wen X, Sun L, Chen Y, Xue P, Yang Q, Wang B, Yu N, Cao Y, Zhang Y, Gong K, Wu W, Chen D, Cao L, Cheng S, Zhang Y, Zhan X (2020) Rice dwarf and low tillering 10 (OsDLT10) regulates tiller number by monitoring auxin homeostasis. Plant Sci 297:110502. https://doi.org/10.1016/j.plantsci.2020.110502

    CAS  Article  PubMed  Google Scholar 

  102. Xing Y, Zhang Q (2010) Genetic and molecular bases of rice yield. Annu Rev Plant Biol 61:421–442

    CAS  PubMed  Article  Google Scholar 

  103. Xu J, Xiong W, Cao B, Yan T, Luo T, Fan T, Luo M (2013) Molecular characterization and functional analysis of “fruit-weight 2.2-like” gene family in rice. Planta 238:643–655

    CAS  PubMed  Article  Google Scholar 

  104. Xu R, Yang Y, Qin R, Li H, Qiu C, Li L, Wei P, Yang J (2016) Rapid improvement of grain weight via highly efficient CRISPR/Cas9-mediated multiplex genome editing in rice. J Genet Genomics 43:529–532

    PubMed  Article  Google Scholar 

  105. Xu L, Yuan K, Yuan M, Meng X, Chen M, Wu J, Li J, Qi Y (2020) Regulation of rice tillering by RNA-directed DNA methylation at miniature inverted-repeat transposable elements. Mol Plant 13:851–863

    CAS  PubMed  Article  Google Scholar 

  106. Yang XC, Hwa CM (2008) Genetic modification of plant architecture and variety improvement in rice. Heredity 101:396–404

    CAS  PubMed  Article  Google Scholar 

  107. Yang Q, Zhong X, Li Q, Lan J, Tang H, Qi P, Ma J, Wang J, Chen G, Pu Z, Li W, Lan X, Deng M, Harwood W, Li Z, Wei Y, Zheng Y, Jiang Q (2020) Mutation of the D-hordein gene by RNA-guided Cas9 targeted editing reducing the grain size and changing grain compositions in barley. Food Chem 311:125892. https://doi.org/10.1016/j.foodchem.2019.125892

    CAS  Article  PubMed  Google Scholar 

  108. Yano K, Ookawa T, Aya K, Ochiai Y, Hirasawa T, Ebitani T, Takarada T, Yano M, Yamamoto T, Fukuoka S, Wu J, Ando T, Ordonio RL, Hirano K, Matsuoka M (2015) Isolation of a novel lodging resistance QTL gene involved in strigolactone signaling and its pyramiding with a QTL gene involved in another mechanism. Mol Plant 8:303–314

    CAS  PubMed  Article  Google Scholar 

  109. Yin W, Xiao Y, Niu M, Meng W, Li L, Zhang X, Liu D, Zhang G, Qian Y, Sun Z, Huang R, Wang S, Liu CM, Chu C, Tong H (2020) ARGONAUTE2 enhances grain length and salt tolerance by activating BIG GRAIN3 to modulate cytokinin distribution in rice. Plant Cell 32:2292–2306

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  110. Yu XL, Wang HY, Leung DWM, He ZD, Zhang JJ, Peng XX, Liu EE (2019) Overexpression of OsIAAGLU reveals a role for IAA-glucose conjugation in modulating rice plant architecture. Plant Cell Rep 38:731–739

    CAS  PubMed  Article  Google Scholar 

  111. Yu X, Xia S, Xu Q, Cui Y, Gong M, Zeng D, Zhang Q, Shen L, Jiao G, Gao Z, Hu J, Zhang G, Zhu L, Guo L, Ren D, Qian Q (2020) ABNORMAL FLOWER AND GRAIN 1 encodes OsMADS6 and determines palea identity and affects rice grain yield and quality. Sci China Life Sci 63:228–238

    CAS  PubMed  Article  Google Scholar 

  112. Zeng Y, Wen J, Zhao W, Wang Q, Huang W (2020) Rational improvement of rice yield and cold tolerance by editing the three genes OsPIN5b, GS3, and OsMYB30 with the CRISPR-Cas9 system. Front Plant Sci 10:1663. https://doi.org/10.3389/fpls.2019.01663

    Article  PubMed  PubMed Central  Google Scholar 

  113. Zhang Y, Liang Z, Zong Y, Wang Y, Liu J, Chen K, Qiu JL, Gao C (2016) Efficient and transgene-free genome editing in wheat through transient expression of CRISPR/Cas9 DNA or RNA. Nat Commun 7:12617. https://doi.org/10.1038/ncomms12617

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  114. Zhang Y, Li D, Zhang D, Zhao X, Cao X, Dong L, Liu J, Chen K, Zhang H, Gao C, Wang D (2018) Analysis of the functions of TaGW2 homoeologs in wheat grain weight and protein content traits. Plant J 94:857–866

    CAS  PubMed  Article  Google Scholar 

  115. Zhang Z, Hua L, Gupta A, Tricoli D, Edwards KJ, Yang B, Li W (2019) Development of an Agrobacterium-delivered CRISPR/Cas9 system for wheat genome editing. Plant Biotechnol J 17:1623–1635

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  116. Zhang J, Zhang X, Chen R, Yang L, Fan K, Liu Y, Wang G, Ren Z, Liu Y (2020) Generation of transgene-free semidwarf maize plants by gene editing of gibberellin-oxidase20-3 using CRISPR/Cas9. Front Plant Sci 11:1048. https://doi.org/10.3389/fpls.2020.01048

    Article  PubMed  PubMed Central  Google Scholar 

  117. Zhao Q, Feng Q, Lu H, Li Y, Wang A, Tian Q, Zhan Q, Lu Y, Zhang L, Huang T, Wang Y, Fan D, Zhao Y, Wang Z, Zhou C, Chen J, Zhu C, Li W, Weng Q, Xu Q, Wang ZX, Wei X, Han B, Huang X (2018) Pan-genome analysis highlights the extent of genomic variation in cultivated and wild rice. Nature Genet 50:278–284

    CAS  PubMed  Article  Google Scholar 

  118. Zhao M, Tang S, Zhang H, He M, Liu J, Zhi H, Sui Y, Liu X, Jia G, Zhao Z, Yan J, Zhang B, Zhou Y, Chu J, Wang X, Zhao B, Tang W, Li J, Wu C, Liu X, Diao X (2020) DROOPY LEAF1 controls leaf architecture by orchestrating early brassinosteroid signaling. Proc Natl Acad Sci USA. https://doi.org/10.1073/pnas.2002278117

    Article  PubMed  Google Scholar 

  119. Zhou J, Xin X, He Y, Chen H, Li Q, Tang X, Zhong Z, Deng K, Zheng X, Akher SA, Cai G, Qi Y, Zhang Y (2019) Multiplex QTL editing of grain-related genes improves yield in elite rice varieties. Plant Cell Rep 38:475–485

    CAS  PubMed  Article  Google Scholar 

  120. Zhu C, Bortesi L, Baysal C, Twyman RM, Fischer R, Capell T, Schillberg S, Christou P (2017) Characteristics of genome editing mutations in cereal crops. Trends Plant Sci 22:38–52

    CAS  PubMed  Article  Google Scholar 

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Acknowledgements

This work was supported by the Spanish Ministry of Economy and Competitiveness (MINECO), Spain (RTI2018-097613-B-I00; PGC2018-097655-B-I00); PROSTRIG, ERA-NET Cofund SusCrop (Grant N°771134); and the Austrian Science Fund FWF (I2823-B25).

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CZ, ES and PC conceived and designed the review. CZ, XH, JH, ES and PC wrote the manuscript. All authors read and approved the manuscript.

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Correspondence to Changfu Zhu.

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Huang, X., Hilscher, J., Stoger, E. et al. Modification of cereal plant architecture by genome editing to improve yields. Plant Cell Rep (2021). https://doi.org/10.1007/s00299-021-02668-7

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Keywords

  • Cereal crops
  • CRISPR/Cas
  • Genome editing
  • Grain yield
  • Plant architecture