Skip to main content

Advertisement

Log in

CRISPR/Cas-mediated genome editing in sorghum — recent progress, challenges and prospects

  • Special Issue on Genome Editing
  • Published:
In Vitro Cellular & Developmental Biology - Plant Aims and scope Submit manuscript

Abstract

Sorghum is a versatile crop with great potential as a sustainable food, feed, and bioenergy source. To mitigate the severely negative impact of climate change and population growth on food and energy security, further elevation of the crops stress tolerance is urgently needed. Genome editing technologies such as CRISPR/Cas have great potential to accelerate functional genomics and crop improvement by supporting targeted modification of almost any crop gene sequence. We describe the recent progress in genome editing of sorghum. In addition, we review remaining challenges and prospects of emerging gene editing technologies for rapid precision breeding of this crop.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1.

Similar content being viewed by others

References

  • Abel S, Theologis A (1994) Transient transformation of Arabidopsis leaf protoplasts: a versatile experimental system to study gene expression. Plant J 5:421–427

    Article  CAS  PubMed  Google Scholar 

  • Ali Z, Abul-Faraj A, Li L, Ghosh N, Piatek M, Mahjoub A, Aouida M, Piatek A, Baltes NJ, Voytas DF, Dinesh-Kumar S, Mahfouz MM (2015) Efficient virus-mediated genome editing in plants using the CRISPR/Cas9 system. Mol Plant 8:1288–1291

    Article  CAS  PubMed  Google Scholar 

  • Altpeter F, Springer NM, Bartley LE, Blechl AE, Brutnell TP, Citovsky V, Conrad LJ, Gelvin SB, Jackson DP, Kausch AP, Lemaux PG, Medford JI, Orozco-Cárdenas ML, Tricoli DM, Van Eck J, Voytas DF, Walbot V, Wang K, Zhang ZJ, Stewart CN Jr (2016) Advancing crop transformation in the era of genome editing. Plant Cell 28:1510–1520

    CAS  PubMed  PubMed Central  Google Scholar 

  • Anzalone AV, Randolph PB, Davis JR, Sousa AA, Koblan LW, Levy JM, Chen PJ, Wilson C, Newby GA, Raguram A, Liu DR (2019) Search-and-replace genome editing without double-strand breaks or donor DNA. Nature 576:149–157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anzalone AV, Koblan LW, Liu DR (2020) Genome editing with CRISPR–Cas nucleases, base editors, transposases and prime editors. Nat Biotechnol 38:824–844

    Article  CAS  PubMed  Google Scholar 

  • Basak J, Nithin C (2015) Targeting non-coding RNAs in plants with the CRISPR-Cas technology is a challenge yet worth accepting. Front Plant Sci 6:1001

    Article  PubMed  PubMed Central  Google Scholar 

  • Bhaskaran S, Smith RH (1988) Enhanced somatic embryogenesis in Sorghum bicolor from shoot tip culture. In Vitro Cell Dev Biol Plant 24:65–70

  • Bibikova M, Beumer K, Trautman JK, Carroll D (2003) Enhancing gene targeting with designed zinc finger nucleases. Science 300:764

    Article  CAS  PubMed  Google Scholar 

  • Boch J, Scholze H, Schornack S, Landgraf A, Hahn S, Kay S, Lahaye T, Nickstadt A, Bonas U (2009) Breaking the code of DNA binding specificity of TAL-type III effectors. Science 326:1509–1512

    Article  CAS  PubMed  Google Scholar 

  • Bossche RV, Demedts B, Vanderhaeghen R, Goossens A (2013) Transient expression assays in tobacco protoplasts. Methods Mol Biol 1011:227–239

    Article  CAS  Google Scholar 

  • Brant EJ, Baloglu MC, Parikh A, Altpeter F (2021) CRISPR/Cas9 mediated targeted mutagenesis of LIGULELESS-1 in sorghum provides a rapidly scorable phenotype by altering leaf inclination angle. Biotechnol J, accepted for publication

  • Brant EJ, Budak H (2018) Plant small non-coding RNAs and their roles in biotic stresses. Front Plant Sci 9:1038

    Article  PubMed  PubMed Central  Google Scholar 

  • Butt H, Eid A, Momin AA, Bazin J, Crespi M, Arold ST, Mahfouz MM (2019) CRISPR directed evolution of the spliceosome for resistance to splicing inhibitors. Genome Biol 20:1–9

    Article  Google Scholar 

  • Calvino M, Bruggmann R, Messing J (2011) Characterization of the small RNA component of the transcriptome from grain and sweet sorghum stems. BMC Genomics 12:356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Calvino M, Messing J (2012) Sweet sorghum as a model system for bioenergy crops. Curr Opin Biotechnol 23:323–329

    Article  CAS  PubMed  Google Scholar 

  • Can ND, Yoshida T (1999) Genotypic and phenotypic variances and covariances in early maturing grain sorghum in a double cropping. Plant Prod Sci 2:67–70

    Article  Google Scholar 

  • Casas AM, Kononowicz AK, Zehr UB, Tomes DT, Axtell JD, Butler LG, Bressan RA, Hasegawa PM (1993) Transgenic sorghum plants via microprojectile bombardment. Proc Natl Acad Sci U S A 90:11212–11216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Čermák T, Curtin SJ, Gil-Humanes J, Čegan R, Kono TJ, Konečná E, Belanto JJ, Starker CG, Mathre JW, Greenstein RL, Voytas DF (2017) A multipurpose toolkit to enable advanced genome engineering in plants. Plant Cell 29:1196–1217

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chang H, Yi B, Ma R, Zhang X, Zhao H, Xi Y (2016) CRISPR/Cas9, a novel genomic tool to knock down microRNA in vitro and in vivo. Sci Rep 6:22312

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Char SN, Lee H, Yang B (2020b) Use of CRISPR/Cas9 for targeted mutagenesis in sorghum. Curr Protoc Plant Biol 5:e20112

    Article  CAS  PubMed  Google Scholar 

  • Char SN, Wei J, Mu Q, Li X, Zhang ZJ, Yu J, Yang B (2020a) An Agrobacterium-delivered CRISPR/Cas9 system for targeted mutagenesis in sorghum. Plant Biotechnol J 18:319–321

    Article  PubMed  Google Scholar 

  • Che P, Anand A, Wu E, Sander JD, Simon MK, Zhu W, Sigmund AL, Zastrow-Hayes G, Miller M, Liu D, Lawit SJ, Zhao Z-Y, Albertsen MC, Jones TJ (2018) Developing a flexible, high-efficiency Agrobacterium-mediated sorghum transformation system with broad application. Plant Biotechnol J 16:1388–1395

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Che P, Wu E, Simon MK, Anand A, Lowe K, Gao H, Sigmund AL, Yang M, Albertsen MC, Gordon-Kamm W, Jones TJ (2021) Wuschel2 enables highly efficient CRISPR/Cas-targeted genome editing during rapid de novo shoot regeneration in sorghum. bioRxiv 449302.

  • Chung PJ, Chung H, Oh N, Choi J, Bang SW, Jung SE, Jung H, Shim JS, Kim JK (2020) Efficiency of recombinant CRISPR/rCas9-mediated miRNA gene editing in rice. Int J Mol Sci 21:9606

    Article  CAS  PubMed Central  Google Scholar 

  • Cifuentes R, Bressani R, Rolz C (2014) The potential of sweet sorghum as a source of ethanol and protein. Energy Sustain Dev 21:13–19

    Article  CAS  Google Scholar 

  • Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jiang W, Marraffini LA, Zhang F (2013) Multiplex genome engineering using CRISPR/Cas systems. Science 339:819–823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • da Silva MJ, Carneiro PCS, de Souza Carneiro JE, Damasceno CMB, Parrella NNLD, Pastina MM, Simeone MLF, Schaffert RE, da Costa Parrella RA (2018) Evaluation of the potential of lines and hybrids of biomass sorghum. Ind Crop Prod 125:379–385

    Article  CAS  Google Scholar 

  • Dahlberg J, Berenji J, Sikora V, Latkovic D (2011) Assessing sorghum [Sorghum bicolor (L) Moench] germplasm for new traits: food, fuels & unique uses. Maydica 56:85–92

    Google Scholar 

  • de Pater S, Klemann BJ, Hooykaas PJ (2018) True gene-targeting events by CRISPR/Cas-induced DSB repair of the PPO locus with an ectopically integrated repair template. Sci Rep 8:1–10

    Article  CAS  Google Scholar 

  • Dhaka N, Sharma R (2017) MicroRNAs as targets for engineering biofuel feedstock Sorghum. Indian J Plant Physiol 22:484–492

    Article  CAS  Google Scholar 

  • Dong H, Huang Y, Wang K (2021) The development of herbicide resistance crop plants using CRISPR/Cas9-mediated gene editing. Genes 12:912

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Elhag H, Butler LG (1992) Effect of genotype, explant age and medium composition on callus production and plant-regeneration from immature embryos of sorghum. Arab Gulf J Sci Res 10:109–119

    Google Scholar 

  • Erickson JE, Woodard KR, Sollenberger LE (2012) Optimizing sweet sorghum production for biofuel in the southeastern USA through nitrogen fertilization and top removal. BioEnergy Res 5:86–94

    Article  Google Scholar 

  • Galassi E, Taddei F, Ciccoritti R, Nocente F, Gazza L (2020) Biochemical and technological characterization of two C4 gluten-free cereals: Sorghum bicolor and Eragrostis tef. Cereal Chem 97:65–73

    Article  CAS  Google Scholar 

  • Gallego-Bartolomé J, Gardiner J, Liu W, Papikian A, Ghoshal B, Kuo HY, Zhao JM, Segal DJ, Jacobsen SE (2018) Targeted DNA demethylation of the Arabidopsis genome using the human TET1 catalytic domain. Proc Natl Acad Sci U S A 115:E2125–E2134

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gao C (2021) Genome engineering for crop improvement and future agriculture. Cell 184:1621–1635

    Article  CAS  PubMed  Google Scholar 

  • Garneau JE, Dupuis MÈ, Villion M, Romero DA, Barrangou R, Boyaval P, Fremaux C, Horvath P, Magadán AH, Moineau S (2010) The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature 468:67–71

    Article  CAS  PubMed  Google Scholar 

  • Gilbert LA, Larson MH, Morsut L, Liu Z, Brar GA, Torres SE, Stern-Ginossar N, Brandman O, Whitehead EH, Doudna JA, Lim WA, Qi LS (2013) CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes. Cell 154:442–451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gionfriddo M, De Gara L, Loreto F (2019) Directed evolution of plant processes: towards a green (r) evolution? Trends Plant Sci 24:999–1007

    Article  CAS  PubMed  Google Scholar 

  • Gupta S, Kumar A, Patel R, Kumar V (2021) Genetically modified crop regulations: scope and opportunity using the CRISPR-Cas9 genome editing approach. Mol Biol Rep 1-13.

  • Gurel S, Gurel E, Kaur R, Wong J, Meng L, Tan HQ, Lemaux PG (2009) Efficient, reproducible Agrobacterium-mediated transformation of sorghum using heat treatment of immature embryos. Plant Cell Rep 28:429–444

    Article  CAS  PubMed  Google Scholar 

  • Hamza NB, Sharma N, Tripathi A, Sanan-Mishra N (2016) MicroRNA expression profiles in response to drought stress in Sorghum bicolor. Gene Expr Patterns 20:88–98

    Article  CAS  PubMed  Google Scholar 

  • Hao H, Li Z, Leng C, Lu C, Luo H, Liu Y, Wu X, Liu Z, Shang L, Jing HC (2021) Sorghum breeding in the genomic era: opportunities and challenges. Theor Appl Genet 1-26

  • Hilbeck A, Meyer H, Wynne B, Millstone E (2020) GMO regulations and their interpretation: how EFSA’s guidance on risk assessments of GMOs is bound to fail. Environ Sci Eur 32:1–15

    Article  Google Scholar 

  • Hong Y, Meng J, He X, Zhang Y, Liu Y, Zhang C, Qi H, Luan Y (2020) Editing miR482b and miR482c simultaneously by CRISPR/Cas9 enhanced tomato resistance to Phytophthora infestans. Phytopathology (in press)

  • Howe A, Sato S, Dweikat I, Fromm M, Clemente T (2006) Rapid and reproducible Agrobacterium-mediated transformation of sorghum. Plant Cell Rep 25:784–791

    Article  CAS  PubMed  Google Scholar 

  • Huang TK, Puchta H (2019) CRISPR/Cas-mediated gene targeting in plants: finally a turn for the better for homologous recombination. Plant Cell Rep 38:443–453 

  • Hummel AW, Chauhan RD, Cermak T, Mutka AM, Vijayaraghavan A, Boyher A, Starker CG, Bart R, Voytas DF, Taylor NJ (2018) Allele exchange at the EPSPS locus confers glyphosate tolerance in cassava. Plant Biotechnol J 16:1275–1282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Indra Arulselvi P, Krishnaveni S (2009) Effects of hormones, explants and genotypes in in vitro culturing of sorghum. J Biochem Technol 1:96–103

    Google Scholar 

  • Jiang W, Zhou H, Bi H, Fromm M, Yang B, Weeks DP (2013) Demonstration of CRISPR/Cas9/sgRNA-mediated targeted gene modification in Arabidopsis, tobacco, sorghum and rice. Nucleic Acids Res 20:e188

    Article  CAS  Google Scholar 

  • Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E (2012) A programmable dual-RNA–guided DNA endonuclease in adaptive bacterial immunity. Science 337:816–821

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jogeswar G, Ranadheer D, Anjaiah V, Kishor PK (2007) High frequency somatic embryogenesis and regeneration in different genotypes of Sorghum bicolor (L.) Moench from immature inflorescence explants. In Vitro Cell Dev Biol Plant 43:159–166

  • Jordan DR, Mace ES, Cruickshank AW, Hunt CH, Henzell RG (2011) Exploring and exploiting genetic variation from unadapted sorghum germplasm in a breeding program. Crop Sci 51:1444–1457

    Article  Google Scholar 

  • Kang BC, Yun JY, Kim ST, Shin Y, Ryu J, Choi M, Woo JW, Kim JS (2018) Precision genome engineering through adenine base editing in plants. Nat Plants 4:427–431

    Article  CAS  PubMed  Google Scholar 

  • Khakhar A, Wang C, Swanson R, Stokke S, Rizvi F, Sarup S, Hobbs J, Voytas DF (2021) VipariNama: RNA viral vectors to rapidly elucidate the relationship between gene expression and phenotype. Plant Physiol (in press)

  • Kiani S, Chavez A, Tuttle M, Hall RN, Chari R, Ter-Ovanesyan D, Qian J, Pruitt BW, Beal J, Vora S, Buchthal J, Kowal EJK, Ebrahimkhani MR, Collins JJ, Weiss R, Church G (2015) Cas9 gRNA engineering for genome editing, activation and repression. Nat Methods 12:1051–1054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kimball J, Cui Y, Chen D, Brown P, Rooney WL, Stacey G, Balint-Kurti PJ (2019) Identification of QTL for target leaf spot resistance in Sorghum bicolor and investigation of relationships between disease resistance and variation in the MAMP response. Sci Rep 9:18285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kour S, Pradhan UK (2016) Genetic variability, heritability and expected genetic advance for yield and yield components in forage sorghum [Sorghum bicolor (L.) Moench]. RASHI 1:71–76

    Google Scholar 

  • Kuang Y, Li S, Ren B, Yan F, Spetz C, Li X, Zhou X, Zhou H (2020) Base-editing-mediated artificial evolution of OsALS1 in planta to develop novel herbicide-tolerant rice germplasms. Mol Plant 13:565–572

  • Kumar R, Kaur A, Pandey A, Mamrutha HM, Singh GP (2019) CRISPR-based genome editing in wheat: a comprehensive review and future prospects. Mol Biol Rep 1-13

  • Lee J, Park J-J, Kim SL, Yim J, An G (2007) Mutations in the rice liguleless gene result in a complete loss of the auricle, ligule, and laminar joint. Plant Mol Biol 65:487–499

    Article  CAS  PubMed  Google Scholar 

  • Lee MW, Yang Y (2006) Transient expression assay by agroinfiltration of leaves. Methods Mol Biol 323:225–229

    PubMed  Google Scholar 

  • Leff B, Ramankutty N, Foley JA (2004) Geographic distribution of major crops across the world. Global Biogeochem Cy 20:1000–1029

    Google Scholar 

  • Li A, Jia S, Yobi A, Ge Z, Sato SJ, Zhang C, Angelovici R, Clemente TE, Holding DR (2018a) Editing of an alpha-kafirin gene family increases, digestibility and protein quality in sorghum. Plant Physiol 177:1425–1438

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li C, Zhang R, Meng X, Chen S, Zong Y, Lu C, Qiu JL, Chen YH, Li J, Gao C (2020) Targeted, random mutagenesis of plant genes with dual cytosine and adenine base editors. Nat Biotechnol 38:875–882

    Article  CAS  PubMed  Google Scholar 

  • Li C, Zong Y, Wang Y, Jin S, Zhang D, Song Q, Zhang R, Gao C (2018b) Expanded base editing in rice and wheat using a Cas9-adenosine deaminase fusion. Genome Biol 19:1–9

    Article  CAS  Google Scholar 

  • Li Z, Zhang D, Xiong X, Yan B, Xie W, Sheen J, Li JF (2017) A potent Cas9-derived gene activator for plant and mammalian cells. Nat Plants 3:930–936

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liang L, Deng L, Chen Y, Li GC, Shao C, Tischfield JA (2005) Modulation of DNA end joining by nuclear proteins. J Biol Chem 280:31442–31449

    Article  CAS  PubMed  Google Scholar 

  • Liang Z, Chen K, Li T, Zhang Y, Wang Y, Zhao Q, Liu J, Zhang H, Liu C, Ran Y, Gao C (2017) Efficient DNA-free genome editing of bread wheat using CRISPR/Cas9 ribonucleoprotein complexes. Nat Commun 8:1–5

    Article  CAS  Google Scholar 

  • Lin Q, Zong Y, Xue C, Wang S, Jin S, Zhu Z, Wang Y, Anzalone AV, Raguram A, Doman JL, Liu DR, Gao C (2020) Prime genome editing in rice and wheat. Nat Biotechnol 38:582–585

    Article  CAS  PubMed  Google Scholar 

  • Liu G, Gilding EK, Godwin ID (2015) A robust tissue culture system for sorghum [Sorghum bicolor (L.) Moench]. S Afr J Bot 98:157–160

    Article  CAS  Google Scholar 

  • Liu G, Li J, Godwin ID (2019) Genome editing by CRISPR/Cas9 in sorghum through biolistic bombardment. Methods Mol Biol 1931:169–183

    Article  CAS  PubMed  Google Scholar 

  • Liu L, Kuang Y, Yan F, Li S, Ren B, Gosavi G, Spetz C, Li X, Wang X, Zhou X, Zhou H (2020a) Developing a novel artificial rice germplasm for dinitroaniline herbicide resistance by base editing of OsTubA2. Plant Biotechnol J 19:5–7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu X, Qin R, Li J, Liao S, Shan T, Xu R, Wu D, Wei P (2020b) A CRISPR-Cas9-mediated domain-specific base-editing screen enables functional assessment of ACCase variants in rice. Plant Biotechnol J 18:1845–1847

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lowder LG, Zhang D, Baltes NJ, Paul JW, Tang X, Zheng X, Voytas DF, Hsieh TF, Zhang Y, Qi Y (2015) A CRISPR/Cas9 toolbox for multiplexed plant genome editing and transcriptional regulation. Plant Physiol 169:971–985

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lowder LG, Zhou J, Zhang Y, Malzahn A, Zhong Z, Hsieh TF, Voytas DF, Zhang Y, Qi Y (2018) Robust transcriptional activation in plants using multiplexed CRISPR-Act2. 0 and mTALE-Act systems. Mol Plant 11:245–256

    Article  CAS  PubMed  Google Scholar 

  • Lowe K, Wu E, Wang N, Hoerster G, Hastings C, Cho MJ, Scelonge C, Lenderts B, Chamberlin M, Cushatt J, Wang L, Ryan L, Khan T, Chow-Yiu J, Hua W, Yu M, Banh J, Bao Z, Brink K, Igo E, Rudrappa B, Shamseer PM, Bruce W, Newman L, Shen B, Zheng P, Bidney D, Falco C, Register J, Zhao ZY, Xu D, Jones T, Gordon-Kamm W (2016) Morphogenic regulators Baby boom and Wuschel improve monocot transformation. Plant Cell 28:1998–2015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma X, Liu YG (2016) CRISPR/Cas9-based multiplex genome editing in monocot and dicot plants. Curr Protoc Mol Biol 115:31–36

    Article  PubMed  Google Scholar 

  • Mahas A, Ali Z, Tashkandi M, Mahfouz MM (2019) Virus-mediated genome editing in plants using the CRISPR/Cas9 system. Methods Mol Biol 1917:311–326

    Article  CAS  PubMed  Google Scholar 

  • Mat Aron NS, Khoo KS, Chew KW, Show PL, Chen WH, Nguyen THP (2020) Sustainability of the four generations of biofuels–a review. Int J Energy Res 44:9266–9282

    Article  CAS  Google Scholar 

  • Mathur S, Umakanth AV, Tonapi VA, Sharma R, Sharma MK (2017) Sweet sorghum as biofuel feedstock: recent advances and available resources. Biotechnol Biofuels 10:146

    Article  PubMed  PubMed Central  Google Scholar 

  • McCormick RF, Truong SK, Sreedasyam A, Jenkins J, Shu S, Sims D, Kennedy M, Amirebrahimi M, Weers BD, McKinley B, Mattison A, Morishige DT, Grimwood J, Schmutz J, Schmutz J, Mullet JE (2018) The Sorghum bicolor reference genome: improved assembly, gene annotations, a transcriptome atlas, and signatures of genome organization. Plant J 93:338–354

    Article  CAS  PubMed  Google Scholar 

  • Meng R, Wang C, Wang L, Liu Y, Zhan Q, Zheng J, Li J (2020) An efficient sorghum protoplast assay for transient gene expression and gene editing by CRISPR/Cas9. PeerJ 8:e10077

    Article  PubMed  PubMed Central  Google Scholar 

  • Miller FR (1984) Registration of RTx 430 sorghum parental line. Crop Sci 24:1224–1224

    Article  Google Scholar 

  • Mookkan M, Nelson-Vasilchik K, Hague J, Zhang ZJ, Kausch AP (2017) Selectable marker independent transformation of recalcitrant maize inbred B73 and sorghum P898012 mediated by morphogenic regulators BABY BOOM and WUSCHEL2. Plant Cell Rep 36:1477–1491

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moscou MJ, Bogdanove AJ (2009) A simple cipher governs DNA recognition by TAL effectors. Science 326:1501

    Article  CAS  PubMed  Google Scholar 

  • Murovec J, Guček K, Bohanec B, Avbelj M, Jerala R (2018) DNA-free genome editing of Brassica oleracea and B. rapa protoplasts using CRISPR-Cas9 ribonucleoprotein complexes. Front Plant Sci 9:1594

    Article  PubMed  PubMed Central  Google Scholar 

  • Oloo B, Maredia K, Mbabazi R (2020) Advancing adoption of genetically modified crops as food and feed in Africa: the case of Kenya. Afr J Biotechnol 19:694–701

    Article  Google Scholar 

  • Oz MT, Altpeter A, Karan R, Merotto Junior A, Altpeter F (2021) CRISPR/Cas9 mediated multi-allelic gene targeting in sugarcane confers herbicide tolerance. Front Genome Ed 3:673566

  • Papikian A, Liu W, Gallego-Bartolomé J, Jacobsen SE (2019) Site-specific manipulation of Arabidopsis loci using CRISPR-Cas9 SunTag systems. Nat Commun 10:1–11

    Article  CAS  Google Scholar 

  • Park J, Choi S, Park S, Yoon J, Park AY, Choe S (2019) DNA-free genome editing via ribonucleoprotein (RNP) delivery of CRISPR/Cas in lettuce. Methods Mol Biol 1917:337–354

    Article  CAS  PubMed  Google Scholar 

  • Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlack H, Haberer G, Hellsten U, Mitros T, Poliakov A, Schmutz J, Spannagl M, Tang H, Wang X, Wicker T, Bharti AK, Chapman J, Feltus FA, Gowik U, Grigoriev IV, Lyons E, Maher CA, Martis M, Narechania A, Otillar RP, Penning BW, Salamov AA, Wang Y, Zhang L, Carpita NC, Freeling M, Gingle AR, Hash CT, Keller B, Klein P, Kresovich S, McCann MC, Ming R, Peterson DG, Rahman M, Ware D, Westhoff P, Mayer KFX, Messing J, Rokshar DS (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457:551–556

    Article  CAS  PubMed  Google Scholar 

  • Porteus MH, Baltimore D (2003) Chimeric nucleases stimulate gene targeting in human cells. Science 300:763

    Article  PubMed  Google Scholar 

  • Powles SB, Yu Q (2010) Evolution in action: plants resistant to herbicides. Annu Rev Plant Biol 61:317–347

    Article  CAS  PubMed  Google Scholar 

  • Puchta H, Dujon B, Hohn B (1993) Homologous recombination in plant cells is enhanced by in vivo induction of double strand breaks into DNA by a site-specific endonuclease. Nucleic Acids Res 21:5034–5040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raghuwanshi A, Birch RG (2010) Genetic transformation of sweet sorghum. Plant Cell Rep 29:997–1005

    Article  CAS  PubMed  Google Scholar 

  • Reddy BV, Ashok Kumar A, Sanjana Reddy P (2010) Recent advances in sorghum improvement research at ICRISAT. Witthayasan Kasetsart 44:499–506

    CAS  Google Scholar 

  • Rodríguez-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

    Article  PubMed  CAS  Google Scholar 

  • Sander JD (2019) Gene editing in sorghum through agrobacterium. Methods Mol Biol 1931:155–168

    Article  CAS  PubMed  Google Scholar 

  • Sapkota S, Boatwright JL, Jordan K, Boyles R, Kresovich S (2020) Identification of novel genomic associations and gene candidates for grain starch content in sorghum. Genes 11:1448

    Article  CAS  PubMed Central  Google Scholar 

  • Schmer MR, Jin VL, Wienhold BJ (2015) Sub-surface soil carbon changes affects biofuel greenhouse gas emissions. Biomass Bioenergy 81:31–34

    Article  CAS  Google Scholar 

  • Schmidt C, Pacher M, Puchta H (2019) DNA break repair in plants and its application for genome engineering. Methods Mol Biol 1864:237–266

    Article  CAS  PubMed  Google Scholar 

  • Shariati SA, Dominguez A, Xie S, Wernig M, Qi LS, Skotheim JM (2019) Reversible disruption of specific transcription factor-DNA interactions using CRISPR/Cas9. Mol Cell 74:622–633

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharma R, Liang Y, Lee MY, Pidatala VR, Mortimer JC, Scheller HV (2020) Agrobacterium-mediated transient transformation of sorghum leaves for accelerating functional genomics and genome editing studies. BMC Res Notes 13:1–7

    Article  Google Scholar 

  • Shimatani Z, Kashojiya S, Takayama M, Terada R, Arazoe T, Ishii H, Teramura H, Yamamoto T, Komatsu H, Miura K, Ezura H, Nishisa K, Ariizumi T, Kondo A (2017) Targeted base editing in rice and tomato using a CRISPR-Cas9 cytidine deaminase fusion. Nat Biotechnol 35:441–443

    Article  CAS  PubMed  Google Scholar 

  • Silva TN, Kelly ME, Vermerris W (2020) Use of Sorghum bicolor leaf whorl explants to expedite regeneration and increase transformation throughput. Plant Cell Tiss Organ Cult 141:243–255

  • Singhvi MS, Gokhale DV (2019) Lignocellulosic biomass: hurdles and challenges in its valorization. Appl Microbiol Biotechnol 103:9305–9320

    Article  CAS  PubMed  Google Scholar 

  • Sun Y, Zhang X, Wu C, He Y, Ma Y, Hou H, Guo X, Du W, Zhao Y, Xia L (2016) Engineering herbicide-resistant rice plants through CRISPR/Cas9-mediated homologous recombination of Acetolactate Synthase. Mol Plant 9:628–361

    Article  CAS  PubMed  Google Scholar 

  • Svitashev S, Schwartz C, Lenderts B, Young JK, Cigan AM (2016) Genome editing in maize directed by CRISPR–Cas9 ribonucleoprotein complexes. Nat Commun 7:13274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tian J, Wang C, Xia J, Wu L, Xu G, Wu W, Li D, Qin W, Han X, Chen Q, Jin W (2019) Teosinte ligule allele narrows plant architecture and enhances high-density maize yield. Science 365:6454

    Article  Google Scholar 

  • Ulukan H (2009) The evolution of cultivated plant species: classical plant breeding versus genetic engineering. Plant Syst Evol 280:133–142

    Article  Google Scholar 

  • Wroblewski T, Tomczak A, Michelmore R (2005) Optimization of Agrobacterium-mediated transient assays of gene expression in lettuce, tomato and Arabidopsis. Plant Biotechnol J 3:259–273

    Article  CAS  PubMed  Google Scholar 

  • Xing HL, Dong L, Wang ZP, Zhang HY, Han CY, Liu B, Wang XC, Chen QJ (2014) A CRISPR/Cas9 toolkit for multiplex genome editing in plants. BMC Plant Biol 14:1–12

    Article  CAS  Google Scholar 

  • Xu R, Li J, Liu X, Shan T, Qin R, Wei P (2020a) Development of plant prime-editing systems for precise genome editing. Plant Commun 1:100043

    Article  PubMed  PubMed Central  Google Scholar 

  • Xu W, Zhang C, Yang Y, Zhao S, Kang G, He X, Song J, Yang J (2020b) Versatile nucleotides substitution in plant using an improved prime editing system. Mol Plant 13:675–678

    Article  CAS  PubMed  Google Scholar 

  • Yang Y, Li R, Qi M (2001) In vivo analysis of plant promoters and transcription factors by agroinfiltration of tobacco leaves. Plant J 22:543–551

    Article  Google Scholar 

  • Zhang D, Hussain A, Manghwar H, Xie K, Xie S, Zhao S, Larkin RM, Qing P, Jin S, Ding F (2020) Genome editing with the CRISPR-Cas system: an art, ethics and global regulatory perspective. Plant Biotechnol J 18:1651–1669

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang R, Liu J, Chai Z, Chen S, Bai Y, Zong Y, Chen K, Li J, Jiang L, Gao C (2019) Generation of herbicide tolerance traits and a new selectable marker in wheat using base editing. Nat Plants 5:480–485

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Massel K, Godwin ID, Gao C (2018) Applications and potential of genome editing in crop improvement. Genome Biol 19:210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao ZY, Cai T, Tagliani L, Miller M, Wang N, Pang H, Rudert M, Schroeder S, Hondred D, Seltzer J, Pierce D (2000) Agrobacterium-mediated sorghum transformation. Plant Mol Biol 44:789–798

    Article  CAS  PubMed  Google Scholar 

  • Zhong H, Wang W, Sticklen M (1998) In vitro morphogenesis of Sorghum bicolor (L.) Moench: efficient plant regeneration from shoot apices. J Plant Physiol 153:719–726

    Article  CAS  Google Scholar 

  • Zhou J, Deng K, Cheng Y, Zhong Z, Tian L, Tang X, Tang A, Zheng X, Zhang T, Qi Y, Zhang Y (2017) CRISPR_Cas9 based genome editing reveals new insights into microRNA function and regulation in rice. Front Plant Sci 8:1598

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhu H, Li C, Gao C (2020) Applications of CRISPR–Cas in agriculture and plant biotechnology. Nat Rev Mol Cell Biol 21:661–677

    Article  CAS  PubMed  Google Scholar 

  • Zong Y, Wang Y, Li C, Zhang R, Chen K, Ran Y, Qiu JL, Wang D, Gao C (2017) Precise base editing in rice, wheat and maize with a Cas9-cytidine deaminase fusion. Nat Biotechnol 35:438–440

    Article  CAS  PubMed  Google Scholar 

  • Zong Y, Song Q, Li C, Jin S, Zhang D, Wang Y, Qiu JL, Gao C (2018) Efficient C-to-T base editing in plants using a fusion of nCas9 and human APOBEC3A. Nat Biotechnol 36:950–953

    Article  CAS  Google Scholar 

Download references

Funding

This review was partially funded by the DOE Center for Advanced Bioenergy and Bioproducts Innovation (U.S. Department of Energy, Office of Science, Office of Biological and Environmental Research) under award number DE-SC0018420.

Author information

Authors and Affiliations

Authors

Contributions

AP and EB contributed equally to this manuscript and should be considered joint first authors. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Fredy Altpeter.

Ethics declarations

Disclaimer

Any opinions, findings and conclusions, or recommendations expressed in this publication are those of the authors and do not necessarily reflect the views of the U.S. Department of Energy.

Additional information

Editor: David Songstad

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Parikh, A., Brant, E.J., Baloglu, M.C. et al. CRISPR/Cas-mediated genome editing in sorghum — recent progress, challenges and prospects. In Vitro Cell.Dev.Biol.-Plant 57, 720–730 (2021). https://doi.org/10.1007/s11627-021-10215-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11627-021-10215-y

Keywords

Navigation