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1. Genome evolution and diversity of wild and cultivated potatoes

   https://doi.org/10.1038/s41586-022-04822-x  

   Tang, Dié ; Jia, Yuxin ; Zhang, Jinzhe ; Li, Hongbo ; Cheng, Lin ; Wang, Pei ; Bao, Zhigui ; Liu, Zhihong ; Feng, Shuangshuang ; Zhu, Xijian ; et al ( June 2022 , Nature)

   Abstract Potato ( Solanum tuberosum L.) is the world’s most important non-cereal food crop, and the vast majority of commercially grown cultivars are highly heterozygous tetraploids. Advances in diploid hybrid breeding based on true seeds have the potential to revolutionize future potato breeding and production 1–4 . So far, relatively few studies have examined the genome evolution and diversity of wild and cultivated landrace potatoes, which limits the application of their diversity in potato breeding. Here we assemble 44 high-quality diploid potato genomes from 24 wild and 20 cultivated accessions that are representative of Solanum section Petota , the tuber-bearing clade, as well as 2 genomes from the neighbouring section, Etuberosum . Extensive discordance of phylogenomic relationships suggests the complexity of potato evolution. We find that the potato genome substantially expanded its repertoire of disease-resistance genes when compared with closely related seed-propagated solanaceous crops, indicative of the effect of tuber-based propagation strategies on the evolution of the potato genome. We discover a transcription factor that determines tuber identity and interacts with the mobile tuberization inductive signal SP6A. We also identify 561,433 high-confidence structural variants and construct a map of large inversions, which provides insights for improving inbred lines and precluding potential linkage drag, as exemplified by a 5.8-Mb inversion that is associated with carotenoid content in tubers. This study will accelerate hybrid potato breeding and enrich our understanding of the evolution and biology of potato as a global staple food crop. 

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2. TAL Effectors with Avirulence Activity in African Strains of Xanthomonas oryzae pv. oryzae

   https://doi.org/10.1186/s12284-022-00553-9  

   Lachaux, Marlène ; Thomas, Emilie ; Bogdanove, Adam J. ; Szurek, Boris ; Hutin, Mathilde ( February 2022 , Rice)

   Xanthomonas oryzaepv.oryzae(Xoo) causes bacterial leaf blight, a devastating disease of rice. Among the type-3 effectors secreted byXooto support pathogen virulence, the Transcription Activator-Like Effector (TALE) family plays a critical role. Some TALEs are major virulence factors that activate susceptibility (S) genes, overexpression of which contributes to disease development. Host incompatibility can result from TALE-induced expression of so-called executor (E) genes leading to a strong and rapid resistance response that blocks disease development. In that context, the TALE functions as an avirulence (Avr) factor. To date no such avirulence factors have been identified in African strains ofXoo.

   With respect to the importance of TALEs in the Rice-Xoopathosystem, we aimed at identifying those that may act as Avr factor within AfricanXoo. We screened 86 rice accessions, and identified 12 that were resistant to two African strains while being susceptible to a well-studied Asian strain. In a gain of function approach based on the introduction of each of the ninetalgenes of the avirulent African strain MAI1 into the virulent Asian strain PXO99^A, four were found to trigger resistance on specific rice accessions. Loss-of-function mutational analysis further demonstrated theavractivity of two of them,talDandtalI,on the rice varieties IR64 and CT13432 respectively. Further analysis of TalI demonstrated the requirement of its activation domain for triggering resistance in CT13432. Resistance in 9 of the 12 rice accessions that were resistant against AfricanXoospecifically, including CT13432, could be suppressed or largely suppressed by trans-expression of the truncTALEtal2h, similarly to resistance conferred by theXa1gene which recognizes TALEs generally independently of their activation domain.

   We identified and characterized TalD and TalI as two AfricanXooTALEs with avirulence activity on IR64 and CT13432 respectively. Resistance of CT13432 against AfricanXooresults from the combination of two mechanisms, one relying on the TalI-mediated induction of an unknown executor gene and the other on anXa1-like gene or allele.

    

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3. Natural variation for unusual host responses and flagellin‐mediated immunity against Pseudomonas syringae in genetically diverse tomato accessions

   https://doi.org/10.1111/nph.15788  

   Roberts, Robyn ; Mainiero, Samantha ; Powell, Adrian F. ; Liu, Alexander E. ; Shi, Kai ; Hind, Sarah R. ; Strickler, Susan R. ; Collmer, Alan ; Martin, Gregory B. ( April 2019 , New Phytologist)

   The interaction between tomato andPseudomonas syringaepv tomato (Pst) is a well‐developed model for investigating the molecular basis of the plant immune system. There is extensive natural variation inSolanum lycopersicum(tomato) but it has not been fully leveraged to enhance our understanding of the tomato–Pstpathosystem. We screened 216 genetically diverse accessions of cultivated tomato and a wild tomato species for natural variation in their response to three strains ofPst.

   The host response toPstwas investigated using multiplePststrains, tomato accessions with available genome sequences, reactive oxygen species (ROS) assays, reporter genes and bacterial population measurements.

   The screen uncovered a broad range of previously unseen host symptoms in response toPst, and one of these, stem galls, was found to be simply inherited. The screen also identified tomato accessions that showed enhanced responses to flagellin in bacterial population assays and in ROS assays upon exposure to flagellin‐derived peptides, flg22 and flgII‐28. Reporter genes confirmed that the host responses were due primarily to pattern recognition receptor‐triggered immunity.

   This study revealed extensive natural variation in tomato for susceptibility and resistance toPstand will enable elucidation of the molecular mechanisms underlying these host responses.

    

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4. Experimental insect suppression causes loss of induced, but not constitutive, resistance in Solanum carolinense

   https://doi.org/10.1002/ecy.3786  

   Coverdale, Tyler C. ; Agrawal, Anurag A. ( July 2022 , Ecology)

   Spatiotemporal variation in herbivory is a major driver of intraspecific variation in plant defense. Comparatively little is known, however, about how changes in herbivory regime affect the balance of constitutive and induced resistance, which are often considered alternative defensive strategies. Here, we investigated how nearly a decade of insect herbivore suppression affected constitutive and induced resistance in horsenettle (Solanum carolinense), a widespread herbaceous perennial. We allowed replicated horsenettle populations to respond to the presence or absence of herbivores by applying insecticide to all plants in half of 16 field plots. Horsenettle density rapidly increased in response to insecticide treatment, and this effect persisted for at least 4 years after the cessation of herbivore suppression. We subsequently grew half‐sibling families from seeds collected during and shortly after insecticide treatment in a common garden and found strong effects of insect suppression on induced resistance. Feeding trials in field mesocosms with false Colorado potato beetles (Leptinotarsa juncta), a common specialist herbivore, revealed that multiyear herbivore suppression drove rapid attenuation of induced resistance: offspring of plants from insect‐suppression plots exhibited a near‐complete loss of induced resistance to beetles, whereas those from control plots incurred ~70% less damage after experimental induction. Plants from insect‐suppression plots also had ~40% greater constitutive resistance compared with those from control plots, although this difference was not statistically significant. We nonetheless detected a strong trade‐off between constitutive and induced resistance across families. In contrast, the constitutive expression of trypsin inhibitors (TI), an important chemical defense trait in horsenettle, was reduced by 20% in the offspring of plants from insect‐suppression plots relative to those from control plots. However, TIs were induced to an equal extent whether or not insect herbivores had been historically suppressed. Although several defense and performance traits (prickle density, TI concentration, resistance against false Colorado potato beetles and flea beetles, biomass, and seed mass) varied markedly across families, no traits exhibited significant pairwise correlations. Overall, our results indicate that, whereas the divergent responses of multiple defense traits to insect suppression led to comparatively small changes in overall constitutive resistance, they significantly reduced induced resistance against false Colorado potato beetle.

    

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5. A combination of conserved and diverged responses underlies Theobroma cacao’s defense response to Phytophthora palmivora

   https://doi.org/10.1186/s12915-024-01831-2  

   Winters, Noah P. ; Wafula, Eric K. ; Knollenberg, Benjamin J. ; Hämälä, Tuomas ; Timilsena, Prakash R. ; Perryman, Melanie ; Zhang, Dapeng ; Sheaffer, Lena L. ; Praul, Craig A. ; Ralph, Paula E. ; et al ( February 2024 , BMC Biology)

   Plants have complex and dynamic immune systems that have evolved to resist pathogens. Humans have worked to enhance these defenses in crops through breeding. However, many crops harbor only a fraction of the genetic diversity present in wild relatives. Increased utilization of diverse germplasm to search for desirable traits, such as disease resistance, is therefore a valuable step towards breeding crops that are adapted to both current and emerging threats. Here, we examine diversity of defense responses across four populations of the long-generation tree cropTheobroma cacaoL., as well as four non-cacaoTheobromaspecies, with the goal of identifying genetic elements essential for protection against the oomycete pathogenPhytophthora palmivora.

   We began by creating a new, highly contiguous genome assembly for theP. palmivora-resistant genotype SCA 6 (Additional file 1: Tables S1-S5), deposited in GenBank under accessions CP139290-CP139299. We then used this high-quality assembly to combine RNA and whole-genome sequencing data to discover several genes and pathways associated with resistance. Many of these are unique, i.e., differentially regulated in only one of the four populations (diverged 40 k–900 k generations). Among the pathways shared across all populations is phenylpropanoid biosynthesis, a metabolic pathway with well-documented roles in plant defense. One gene in this pathway, caffeoyl shikimate esterase (CSE), was upregulated across all four populations following pathogen treatment, indicating its broad importance for cacao’s defense response. Further experimental evidence suggests this gene hydrolyzes caffeoyl shikimate to create caffeic acid, an antimicrobial compound and known inhibitor ofPhytophthora spp.

   Our results indicate most expression variation associated with resistance is unique to populations. Moreover, our findings demonstrate the value of using a broad sample of evolutionarily diverged populations for revealing the genetic bases of cacao resistance toP. palmivora. This approach has promise for further revealing and harnessing valuable genetic resources in this and other long-generation plants.

    

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