Multiple modes of convergent adaptation in the spread of glyphosate-resistant Amaranthus tuberculatus

Kreiner et al., PNAS, published September 30, 2019

While evolution has been thought of as playing out over millions of years, adaptation to new environments can occur very rapidly, presenting us with key opportunities to understand evolutionary dynamics. One of the most amazing examples of real-time evolution comes from agriculture, where due to the intense use of a few herbicides, many plant species have evolved herbicide resistance to become aggressive weeds. An important question has been whether herbicide resistance arises only rarely and then spreads quickly, or whether herbicide resistance arises all the time de novo. Our work with glyphosate resistance in US Midwestern and Canadian populations of Amaranthus tuberculatus reveals the answer to be, “it depends,” as we surprisingly find examples for both modes of evolution.

Congratulations, everyone!

Our 9-players team and tournament impressions:

Natural selection on the Arabidopsis thaliana genome in present and future climates

Moises Exposito-Alonso, 500 Genomes Field Experiment Team, Hernán A. Burbano, Oliver Bossdorf, Rasmus Nielsen & Detlef Weigel
Nature, published online August 28, 2019

Through the lens of evolution, climate change is an agent of natural selection that forces populations to change and adapt, or face extinction. However, current assessments of the risk of biodiversity associated with climate change do not typically take into account how natural selection influences populations differently depending on their genetic makeup. Here we make use of the extensive genome information that is available for Arabidopsis thaliana and measure how manipulation of the amount of rainfall affected the fitness of 517 natural Arabidopsis lines that were grown in Spain and Germany. This allowed us to directly infer selection along the genome. Natural selection was particularly strong in the hot-dry location in Spain, where 63% of lines were killed and where natural selection substantially changed the frequency of approximately 5% of all genome-wide variants. A significant portion of this climate-driven natural selection of variants was predictable from signatures of local adaptation (R2 = 29–52%), as genetic variants that were found in geographical areas with climates more similar to the experimental sites were positively selected. Field-validated predictions across the species range indicated that Mediterranean and western Siberian populations—at the edges of the environmental limits of this species—currently experience the strongest climate-driven selection. With more frequent droughts and rising temperatures in Europe, we forecast an increase in directional natural selection moving northwards from the southern end of Europe, putting many native A. thaliana populations at evolutionary risk.

We have found issues with our article ‘Sequence and Expression Differences Underlie Functional Specialization of Arabidopsis MicroRNAs miR159 and miR319’, published in Developmental Cell in July 2007.

1. Even though it should be clear from the text, the blot in Figure S10H is the same as the right hand blot in Figure 5H; this information could have been added to the Figure S10H figure legend.

2. The sentence ‘Even the weaker expression of miR319b (which is identical to miR319a) from a 35S:miR319b construct had a pronounced effect on TCP4:GFP RNA levels (Figure 4B)’ in the main text should read ‘Even the weaker expression of miR319b (which is identical to miR319a) from a 35S:miR319b construct had a pronounced effect on TCP4:GFP RNA levels (Figure 4A)’.

3. We noticed spliced lanes in an RNA blot in Figure 4A and Figure S7 that were not mentioned in the figure legend.

We have gone back to the original data, and properly re-assembled Figure S7 with a clear indication of the spliced lanes. A correctly assembled Figure S7 is shown here. (Because spliced gels were not in violation of journal policies at the time of publication, the journal does not judge that this issue requires a formal Correction.)

4. The most serious issue affects Figure 4B. During its assembly, the same image was mistakenly used for the upper and lower left panels of Figure 4B, with one of them rotated by 180°. The two images document experiments performed in 2004, with both panels intended to show similar TCP4:GFP fluorescence signal with or without miR159a overexpression. (There are substantial levels of endogenous miR159a in this tissue, and if miR159a affected TCP4:GFP, we would have expected to see an effect already without miR159a overexpression.)

Unfortunately, the original data of this experiment are no longer available. We have therefore repeated the complete experiment depicted in Figure 4, which includes microscopy images of N benthamiana (Figure 4B) as well as RNA and small RNA blots of the same samples (Figure 4A). TCP4:GFP fluorescence signal was indeed similar with or without miR159a overexpression. A corrected Figure 4 is shown here.

We have discussed this issue with the journal and offered a retraction, since the issue could not be remedied with data available at the time of publication, and since a simple formal Correction is therefore not possible. The journal leadership was of the opinion that retraction of the entire article would go too far, and that they prefer to publish an Editorial Note of Concern regarding these issues. We published a short manuscript describing the repeated experiment with a corrected Figure 4 on bioRxiv, in order to provide a permanent link to these data, and for colleagues to be able to more fully judge the data. We will also mark the paper in our own CVs as having a linked Note of Editorial Concern.

A Species-Wide Inventory of NLR Genes and Alleles in Arabidopsis thaliana

Van de Weyer et al. Cell 178, 1260-1272

Infectious disease is both a major force of selection in nature and a prime cause of yield loss in agriculture. In plants, disease resistance is often conferred by nucleotide-binding leucine-rich repeat (NLR) proteins, intracellular immune receptors that recognize pathogen proteins and their effects on the host. Consistent with extensive balancing and positive selection, NLRs are encoded by one of the most variable gene families in plants, but the true extent of intraspecific NLR diversity has been unclear. Here, we define a nearly complete species-wide pan-NLRome in Arabidopsis thaliana based on sequence enrichment and long-read sequencing. The pan-NLRome largely saturates with approximately 40 well-chosen wild strains, with half of the pan-NLRome being present in most accessions. We chart NLR architectural diversity, identify new architectures, and quantify selective forces that act on specific NLRs and NLR domains. Our study provides a blueprint for defining pan-NLRomes.

RPW8/HR repeats control NLR activation in Arabidopsis thaliana

Barragan et al., PLoS Genetics, published July 25, 2019

In many plant species, conflicts between divergent elements of the immune system, especially nucleotide-binding oligomerization domain-like receptors (NLR), can lead to hybrid necrosis. Here, we report deleterious allele-specific interactions between an NLR and a non-NLR gene cluster, resulting in not one, but multiple hybrid necrosis cases in Arabidopsis thaliana. The NLR cluster is RESISTANCE TO PERONOSPORA PARASITICA 7 (RPP7), which can confer strain-specific resistance to oomycetes. The non-NLR cluster is RESISTANCE TO POWDERY MILDEW 8 (RPW8) / HOMOLOG OF RPW8 (HR), which can confer broad-spectrum resistance to both fungi and oomycetes. RPW8/HR proteins contain at the N-terminus a potential transmembrane domain, followed by a specific coiled-coil (CC) domain that is similar to a domain found in pore-forming toxins MLKL and HET-S from mammals and fungi. C-terminal to the CC domain is a variable number of 21- or 14-amino acid repeats, reminiscent of regulatory 21-amino acid repeats in fungal HET-S. The number of repeats in different RPW8/HR proteins along with the sequence of a short C-terminal tail predicts their ability to activate immunity in combination with specific RPP7 partners. Whether a larger or smaller number of repeats is more dangerous depends on the specific RPW8/HR autoimmune risk variant.