Isai Salas-González

Universidad Nacional Autónoma de México

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Jeffery L. Dangl

University of North Carolina at Chapel Hill

Omri M. Finkel

Hebrew University of Jerusalem

Gabriel Castrillo

University of Nottingham

Corbin D. Jones

University of North Carolina at Chapel Hill

Theresa F. Law

University of North Carolina at Chapel Hill

Paulo José Pereira Lima Teixeira

Universidade de São Paulo

Jonathan M. Conway

Princeton University

Connor R. Fitzpatrick

Huazhong Agricultural University

Cody F. Creech

University of Nebraska–Lincoln

Susannah G. Tringe

Lawrence Berkeley National Laboratory

Cooperative Institutions

University of North Carolina at Chapel Hill

Howard Hughes Medical Institute

University of Nottingham

Universidad Politécnica de Madrid

Donald Danforth Plant Science Center

Centre National de la Recherche Scientifique

Centre for Plant Biotechnology and Genomics

Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria

Duke University

University of Florida

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Schengen-pathway controls spatially separated and chemically distinct lignin deposition in the endodermis

bioRxiv (Cold Spring Harbor Laboratory) (2020)

Guilhem Reyt Priya Ramakrishna Isai Salas-González Satoshi Fujita Ashley Love

ABSTRACT Lignin is a complex polymer precisely deposited in the cell wall of specialised plant cells, where it provides essential cellular functions. Plants coordinate timing, location, abundance and composition of lignin deposition in response to endogenous and exogenous cues. In roots, a fine band of lignin, the Casparian strip encircles endodermal cells. This forms an extracellular barrier to solutes and water and plays a critical role in maintaining nutrient homeostasis. A signalling pathway senses the integrity of this diffusion barrier and can induce over-lignification to compensate for barrier defects. Here, we report that activation of this endodermal sensing mechanism triggers a transcriptional reprogramming strongly inducing the phenylpropanoid pathway and immune signaling. This leads to deposition of compensatory lignin that is chemically distinct from Casparian strip lignin. We also report that a complete loss of endodermal lignification drastically impacts mineral nutrients homeostasis and plant growth.

Endodermis

Phenylpropanoid

Reprogramming

10.1101/2020.10.07.329664

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Persistent legacy effects on soil metagenomes facilitate plant adaptive responses to drought

Authorea (Authorea) (2024)

Nichole Ginnan Valéria Custódio David Gopaulchan Natalie Ford Isai Salas-González

Both chronic and acute drought alter the composition and physiology of soil microbiomes, with implications for globally important processes including carbon cycling and plant productivity. When water is scarce, selection favors microbes with thicker peptidoglycan cell walls, sporulation ability, and constitutive osmolyte production (Schimel, Balser, and Wallenstein 2007)—but also the ability to degrade complex plant-derived polysaccharides, suggesting that the success of plants and microbes during drought are inextricably linked. However, communities vary enormously in their drought responses and subsequent interactions with plants. Hypothesized causes of this variation in drought resilience include soil texture, soil chemistry, and historical precipitation patterns that shaped the starting communities and their constituent species (Evans, Allison, and Hawkes 2022). Currently, the physiological and molecular mechanisms of microbial drought responses and microbe-dependent plant drought responses in diverse natural soils are largely unknown (de Vries et al. 2023). Here, we identify numerous microbial taxa, genes, and functions that characterize soil microbiomes with legacies of chronic water limitation. Soil microbiota from historically dry climates buffered plants from the negative effects of subsequent acute drought, but only for a wild grass species native to the same region, and not for domesticated maize. In particular, microbiota with a legacy of chronic water limitation altered the expression of a small subset of host genes in crown roots, which mediated the effect of acute drought on transpiration and intrinsic water use efficiency. Our results reveal how long-term exposure to water stress alters soil microbial communities at the metagenomic level, and demonstrate the resulting "legacy effects" on neighboring plants in unprecedented molecular and physiological detail.

Drought Tolerance

10.22541/au.172479332.20070170/v1

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A single bacterial genus maintains root growth in a complex microbiome

Nature (2020)

Omri M. Finkel Isai Salas-González Gabriel Castrillo Jonathan M. Conway Theresa F. Law

10.1038/s41586-020-2778-7

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Identification of beneficial and detrimental bacteria that impact sorghum responses to drought using multi-scale and multi-system microbiome comparisons

bioRxiv (Cold Spring Harbor Laboratory) (2021)

Mingsheng Qi Jeffrey C. Berry Kira M. Veley Lily O’Connor Omri M. Finkel

Abstract Background Drought is a major abiotic stress that limits agricultural productivity. Previous field-level experiments have demonstrated that drought decreases microbiome diversity in the root and rhizosphere and may lead to enrichment of specific groups of microbes, such as Actinobacteria . How these changes ultimately affect plant health is not well understood. In parallel, model systems have been used to tease apart the specific interactions between plants and single, or small groups of microbes. However, translating this work into crop species and achieving increased crop yields within noisy field settings remains a challenge. Thus, the next scientific leap forward in microbiome research must cross the great lab-to-field divide. Toward this end, we combined reductionist, transitional and ecological approaches, applied to the staple cereal crop sorghum to identify key beneficial and detrimental, root associated microbes that robustly affect drought stressed plant phenotypes. Results Fifty-three bacterial strains, originally characterized for association with Arabidopsis , were applied to sorghum seeds and their effect on root growth was monitored for seven days. Two Arthrobacter strains, members of the Actinobacteria phylum, caused root growth inhibition (RGI) in Arabidopsis and sorghum. In the context of synthetic communities, strains of Variovorax were able to protect both Arabidopsis and sorghum from the RGI caused by Arthrobacter . As a transitional system, we tested the synthetic communities through a 24-day high-throughput sorghum phenotyping assay and found that during drought stress, plants colonized by Arthrobacter were significantly smaller and had reduced leaf water content as compared to control plants. However, plants colonized by both Arthrobacter and Variovorax performed as well or better than control plants. In parallel, we performed a field trial wherein sorghum was evaluated across well-watered and drought conditions. Drought responsive microbes were identified, including an enrichment in Actinobacteria , consistent with previous findings. By incorporating data on soil properties into the microbiome analysis, we accounted for experimental noise with a newly developed method and were then able to observe that the abundance of Arthrobacter strains negatively correlated with plant growth. Having validated this approach, we cross-referenced datasets from the high-throughput phenotyping and field experiments and report a list of high confidence bacterial taxa that positively associated with plant growth under drought stress. Conclusions A three-tiered experimental system connected reductionist and ecological approaches and identified beneficial and deleterious bacterial strains for sorghum under drought stress.

Arthrobacter

10.1101/2021.04.13.437608

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Unifying comprehensive genomics and transcriptomics in individual cells to illuminate oncogenic and drug resistance mechanisms

bioRxiv (Cold Spring Harbor Laboratory) (2022)

Jeffrey R. Marks Jon S. Zawistowski Isai Salas-González Tia Tate Tatiana V. Morozova

ABSTRACT Discovering transcriptional variation in the absence of underlying genomic contributions hinders understanding of molecular mechanisms of disease. To assess this coordination in individual cells, we leveraged a new workflow, ResolveOME, exploiting the attributes of primary template-directed amplification (PTA) to enable accurate, complete-genome assessment of single-nucleotide variation in conjunction with full-transcript RNA-seq. In cultured AML cells resistant to the FLT3 inhibitor quizartinib, we uncovered a FLT3 missense mutation and matched transcript upregulation of AXL signal transduction and enhancer factor modulation driving resistance. In primary breast cancer cells, we detected oncogenic PIK3CA N345K mutations and heterogeneous classes of chromosomal loss and were empowered to interpret these genotypes with the crucial knowledge of cell identity and state derived from the transcriptome. The study reinforces the plasticity of the genome in conjunction with expected transcriptional modulation, leading to combinatorial alterations that affect cellular evolution that can be identified through application of this workflow to individual cells.

10.1101/2022.04.29.489440

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Involvement of the Rcs regulon in the persistence of SalmonellaTyphimurium in tomatoes

Environmental Microbiology Reports (2016)

Massimiliano Marvasi Marcos H. de Moraes Isai Salas-González Steffen Porwollik Marcelo Alexandre de Farias

It is becoming clear that human enteric pathogens, like Salmonella, can efficiently colonize vegetative and reproductive organs of plants. Even though the bacterium's ability to proliferate within plant tissues has been linked to outbreaks of salmonellosis, little is known about regulatory and physiological adaptations of Salmonella, or other human pathogens, to their persistence in plants. A screen of Salmonella deletion mutants in tomatoes identified rcsA and rcsB genes as those under positive selection. In tomato fruits, populations of Salmonella rcsB mutants were as much as 100-fold lower than those of the wild type. In the follow-up experiments, competitive fitness of rcsA and rcsB mutants was strongly reduced in tomatoes. Bioinformatics predictions identified a putative Salmonella RcsAB binding box (TTMGGAWWAABCTYA) and revealed an extensive putative RcsAB regulon, of which many members were differentially fit within tomatoes.

Regulon

Persistence (discontinuity)

10.1111/1758-2229.12457

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Diverse MarR bacterial regulators of auxin catabolism in the plant microbiome

Carolina Digital Repository (University of North Carolina at Chapel Hill) (2022)

Jonathan M. Conway William G. Walton Isai Salas-González Theresa F. Law Chloe A. Lindberg

Catabolism

10.17615/b1sb-9887

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Correction: Identification of beneficial and detrimental bacteria impacting sorghum responses to drought using multi-scale and multi-system microbiome comparisons

The ISME Journal (2023)

Mingsheng Qi Jeffrey C. Berry Kira M. Veley Lily O’Connor Omri M. Finkel

Identification

10.1038/s41396-023-01442-9

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The Plant Microbiome: From Ecology to Reductionism and Beyond

Annual Review of Microbiology (2020)

Connor R. Fitzpatrick Isai Salas-González Jonathan M. Conway Omri M. Finkel Sarah Gilbert

Methodological advances over the past two decades have propelled plant microbiome research, allowing the field to comprehensively test ideas proposed over a century ago and generate many new hypotheses. Studying the distribution of microbial taxa and genes across plant habitats has revealed the importance of various ecological and evolutionary forces shaping plant microbiota. In particular, selection imposed by plant habitats strongly shapes the diversity and composition of microbiota and leads to microbial adaptation associated with navigating the plant immune system and utilizing plant-derived resources. Reductionist approaches have demonstrated that the interaction between plant immunity and the plant microbiome is, in fact, bidirectional and that plants, microbiota, and the environment shape a complex chemical dialogue that collectively orchestrates the plantmicrobiome. The next stage in plant microbiome research will require the integration of ecological and reductionist approaches to establish a general understanding of the assembly and function in both natural and managed environments.

Reductionism

Plant Immunity

Functional ecology

10.1146/annurev-micro-022620-014327

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Citations (318)

Abstract 6929: Inter- and intratumoral PIK3CA subclonal diversity in breast cancer contextualized by single-cell multiomics

Cancer Research (2024)

Jon S. Zawistowski Isai Salas-González Tia Tate Tatiana Morozova Katherine A. Kennedy

Abstract Rare clonotypes within pre-cancerous tissues can drive progression to cancer. However, the evolution of rare clonotypes in tumors or normal tissue cannot be defined in the absence of single-cell resolution. At this single-cell level, multiomic interrogation across the Central Dogma of Biology provides enhanced power to reconstruct such evolutionary trajectories, defining the mutational profile, cell identify, and receptor expression within each subpopulation. Leveraging a multiomic approach, we aimed to define how different mutations in the same oncogenic driver observed in the same tumor resection associate with copy number variation (CNV) across the genome. We analyzed individual ductal carcinoma in situ/invasive ductal carcinoma cells using a unified whole-genome and full-transcript RNAseq workflow (ResolveOME™, BioSkryb Genomics) coupled with panel-level extracellular protein information through oligo-conjugated antibodies (BioLegend). We sequenced the exomes and transcriptomes of ResolveOME-amplified single cells from mastectomy samples from twelve patients. At the single nucleotide variant (SNV) level, we identified an allelic series of PIK3CA oncogenic driver mutations in the same tumor resection. A single amino acid, in-frame deletion of E109 dominated the sample, followed by H1047R and K111E in decreasing subclonal abundance. A fourth mutation, E345T, not present in the first sample, was detected as the sole PIK3CA variant in the second tumor sample. Intriguingly, each respective PIK3CA mutation class was associated with a distinct copy number alteration profile revealed by low-coverage whole-genome sequencing: Cells harboring the predominant ΔE109 mutation displayed chromosome 8p,16p, and 17 loss while the less abundant H1047R mutation was in single cells harboring 1q gain, 4q loss, and 22 loss in addition to the 8p and 16q loss present in the ΔE109 cells. PIK3CA K111E had a quiescent, 2n copy number profile. The transcriptomic arm of ResolveOME, containing an oligo-conjugated antibody readout of surface protein expression, jointly confirmed the epithelial identity for the cells harboring the oncogenic PIK3CA mutations. A subpopulation of cells harboring prototypical breast cancer CNV were typed as non-epithelial with increased stemness characteristics, indicative of the ability to resolve phenotypic cellular states. These results suggest a tight interrelationship between CNV and SNV influencing the relative rate of clonal expansion. They also provide the opportunity to explore CNV:SNV signature association with loci exclusive of PIK3CA, and to exploit the power of multiomic integration for lineage reconstruction and for defining common oncogenic signatures of the evolving tumors. Citation Format: Jon Zawistowski, Isai Salas-Gonzalez, Tia Tate, Tatiana Morozova, Katherine Kennedy, Durga Arvapalli, Jamie Remington, Jeffrey Marks, E. Shelley Hwang, Gary Harton, Victor Weigman, Jay A. West. Inter- and intratumoral PIK3CA subclonal diversity in breast cancer contextualized by single-cell multiomics [abstract]. In: Proceedings of the American Association for Cancer Research Annual Meeting 2024; Part 1 (Regular Abstracts); 2024 Apr 5-10; San Diego, CA. Philadelphia (PA): AACR; Cancer Res 2024;84(6_Suppl):Abstract nr 6929.

10.1158/1538-7445.am2024-6929

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