Using CRISPR for Targeted Gene Knockout in C. elegans!

Hi everyone,

I am currently working on a project involving C. elegans and looking into using CRISPR to create targeted gene knockouts. I have been reading up on different methods and tools;; but I am a bit confused about the best approach to achieve a clean knockout. Specifically, I am wondering ::-

What is the most efficient guide RNA design strategy for ensuring high specificity in C. elegans: ??
Are there any recommended protocols for minimizing off target effects, particularly for single gene knockouts: ??
Can anyone share their experiences with recovery and verification of homozygous mutants after the knockout: ?? What is the best way to confirm a successful edit: ??

When I searched on the forum for the solution to my query then I found this thread https://community.alliancegenome.org/t/request-for-genes-to-target-for-gfp-knock-in-with-crispr-flutter/ but couldn’t find enough solution.
Any tips, tool recommendations or insights into troubleshooting common challenges would be greatly appreciated !! I am especially interested in hearing about practical experiences from those who have done similar work in C. elegans.

Thanks in advance !!

With Regards,
Derek Theler

To get a clean knockout I would use two guide RNAs (one at the start and one at the end of the gene). To increase the efficiency and ensure a clean knockout, I would provide a 70nt single strand oligonucleotide that is the 35bp upstream and downstream of the gene.

This approach is described in this paper:
Paix, A., Folkmann, A., & Seydoux, G. (2017). Precision genome editing using CRISPR-Cas9 and linear repair templates in C. elegans. Methods , 121–122, 86–93. Redirecting

It’s not quite as good a knock-out as removing all of the coding sequence, but Wang et al's STOP-IN cassette method, using a single CRISPR target anywhere near the start of the coding sequence, might be a bit easier.

For some of your other questions:
I don’t know if it’s “the most efficient guide RNA design strategy” but I’ve had good luck using the “CRISPR Guide RNA Selection Tool” web page at Simon Fraser University.

Standard methods to control for the possibility of off-target effects include making more than one independent allele, and outcrossing. Way back when we did some of the first CRISPR in C. elegans we looked by sequencing, and couldn’t find evidence of frequent off-target effects (there are of course lots of caveats). In general people don’t seem terribly worried about off-target effects (though maybe should be more worried?).

It’s simple to confirm a successful edit by PCR of the resulting locus and Sanger sequencing. It’s important to remember possible heterozygosity, that might go undetected using PCR. In particular, if you use CRISPR to delete your locus, your PCR primers that amplify the deletion version of the locus probably won’t amplify the wild-type locus, which could give you a false impression of homozygosity. Even if the PCR primers you chose can amplify the wild-type locus in a homozygous wild-type animal, the smaller PCR product from the deleted copy can have such an advantage over larger templates in a PCR reaction that they only amplify the deletion version from a heterozygote - or from a more complicated genomic rearrangement containing both wild-type and mutated versions on the same chromosome, which happens on rare occasions. It’s important to include a reaction using PCR primers that can amplify from the wild-type, but not from the deletion version, to ensure its absence. And the reverse is also true: you can have two different CRISPR-induced lesions in your animal, one in each copy of the locus, and if one of those mutant loci has a large deletion or large insertion at the breakpoint it might not amplify using your PCR primers, such that you might think your animals are homozygous for the intended sequence change but they’re actually trans-heterozygous for the intended change and for another, larger change. Balancer chromosomes can also be a useful way to ensure homozygosity.

I echo Hillel on this: while not perfect, the Wang and Sternberg STOP-IN approach - with a 47 bp insertion with a primer landing site - is more economical in reagents and time. If you consider p = probability of a cut at the site of your provided guide RNA, then two cuts in the same chromosome with be p^2. In the two-site gene deletion, if p for each site is 0.10, then the p of two cutting is 0.01. For a STOP-IN it is simply p = 0.1, and so much more efficient: 10% vs. 1%. To unpack that, to be ~99% confident of getting a mutation, for one guide in the above example you’d need to genotype ~40 Rol/dpy-10(cn64) co-CRISPR F1s. For two guides you’d need ~400 animals. So it matters.

Additionally, with STOP-IN one can “shop” for the optimal guide RNA. We usually do this in the first half of the gene, in exons, and biasing toward the 5’ end of the gene. (Remember, you’d like to truncate the resulting protein earlier rather than later, plus Nonsense-Mediated Decay does not work well in the last two exons of a gene. I also avoid locating a guide right next to introns. I don’t know if this avoid use of cryptic splicing, but presumably location in the middle of an exon would minimize that.)

We use a combination of algorithms and chart a middle course: SFU as noted by Hillel, CRISPOR (now at UC Santa Cruz) and WU-CRISPOR. We also use a general principle of shooting for a guide with a GG dinucleotide at positions -1/-2,a s originally predicted by Wang/Sabatini/Lander 2014, Fig 3F. By that, the “ideal” guide is a “GCGG” and the “worst” guide is a “UNUU.” The desirability of a GG has been validated in elegans by Farboud Meyer 2015. With STOP-IN you can shop for these. Our anecdotal experience is that guides based on sequence/algorithms have been much more efficient on average than guides based on location.

Also, we never work with guides with low specificity, e.g. we are usually in the 97-100 range but never less than low 90s using the MIT algorithm. We check predicted off-site targets but that is rarely an issue. For those of us used to dirty old mutagenized backgrounds and familiar with the rate of accumulation of mutations in cultured elegans, CRISPR is a dream of precision. Remember 20-30% of all edits will have misrepairs, but you don’t care with STOP-IN.

For all insertions/deletions, CRISPR, KO consortium or whatever, we use triplex PCR. One primer inside, two flanking. As Hillel notes about sizes: bands compete and not always as expected. Keep your products small (always >500 bp, preferably smaller) and not too different in size from each other. Also, we are VERY fussy about primer design/specificity and use high Tm of 60. We pilot them before the edit but of course you do not have a positive control because you have not yet edited it. For triplex, whenever possible we use three controls single worm lysates: +/+, m/+ and m/m. You would be surprised at how often the products interact in strange ways. For autosomal m/+ simply cross into your mutant and pick het male progeny for lysis. LGX requires another generation and a Dpy or Unc.