What is quantitative plant biology? DOI Creative Commons
Daphné Autran, George W. Bassel, Eunyoung Chae

et al.

Quantitative Plant Biology, Journal Year: 2021, Volume and Issue: 2

Published: Jan. 1, 2021

Abstract Quantitative plant biology is an interdisciplinary field that builds on a long history of biomathematics and biophysics. Today, thanks to high spatiotemporal resolution tools computational modelling, it sets new standard in science. Acquired data, whether molecular, geometric or mechanical, are quantified, statistically assessed integrated at multiple scales across fields. They feed testable predictions that, turn, guide further experimental tests. features such as variability, noise, robustness, delays feedback loops included account for the inner dynamics plants their interactions with environment. Here, we present main this ongoing revolution, through questions around signalling networks, tissue topology, shape plasticity, biomechanics, bioenergetics, ecology engineering. In end, quantitative allows us question better understand our plants. opens door transdisciplinary projects society, notably citizen

Language: Английский

Two NLR immune receptors acquired high-affinity binding to a fungal effector through convergent evolution of their integrated domain DOI Creative Commons
Aleksandra Białas, Thorsten Langner, Adeline Harant

et al.

eLife, Journal Year: 2021, Volume and Issue: 10

Published: July 21, 2021

A subset of plant NLR immune receptors carry unconventional integrated domains in addition to their canonical domain architecture. One example is rice Pik-1 that comprises an heavy metal-associated (HMA) domain. Here, we reconstructed the evolutionary history and its partner, Pik-2, tested hypotheses about adaptive evolution HMA Phylogenetic analyses revealed into before Oryzinae speciation over 15 million years ago has been under diversifying selection. Ancestral sequence reconstruction coupled with functional studies showed two allelic variants independently evolved from a weakly binding ancestral state high-affinity blast fungus effector AVR-PikD. We conclude for most did not sense AVR-PikD, different have recently through distinct biochemical paths produce similar phenotypic outcomes. These findings highlight dynamic nature mechanisms underpinning adaptation pathogens.

Language: Английский

Citations

63

The helper NLR immune protein NRC3 mediates the hypersensitive cell death caused by the cell-surface receptor Cf-4 DOI Creative Commons
Jiorgos Kourelis, Mauricio P. Contreras, Adeline Harant

et al.

PLoS Genetics, Journal Year: 2022, Volume and Issue: 18(9), P. e1010414 - e1010414

Published: Sept. 22, 2022

Cell surface pattern recognition receptors (PRRs) activate immune responses that can include the hypersensitive cell death. However, pathways link PRRs to death response are poorly understood. Here, we show receptor-like protein Cf-4 requires intracellular nucleotide-binding domain leucine-rich repeat containing receptor (NLR) NRC3 trigger a confluent upon detection of fungal effector Avr4 in leaves Nicotiana benthamiana . This activity an intact N-terminal MADA motif, conserved signature coiled-coil (CC)-type plant NLRs is required for resistosome-mediated responses. A chimeric with α1 helix Arabidopsis ZAR1 swapped into retains capacity mediate Pathogen effectors acting as suppressors suppress Cf-4-triggered cell-death. Our findings NLR resistosome model caused by PRR.

Language: Английский

Citations

52

A potato late blight resistance gene protects against multiple Phytophthora species by recognizing a broadly conserved RXLR-WY effector DOI Creative Commons
Xiao Lin, Andrea Olave-Achury,

Robert Heal

et al.

Molecular Plant, Journal Year: 2022, Volume and Issue: 15(9), P. 1457 - 1469

Published: July 31, 2022

Species of the genus Phytophthora, plant killer, cause disease and reduce yields in many crop plants. Although Resistance to Phytophthora infestans (Rpi) genes effective against potato late blight have been cloned, few cloned other species. Most Rpi encode nucleotide-binding domain, leucine-rich repeat-containing (NLR) immune receptor proteins that recognize RXLR (Arg-X-Leu-Arg) effectors. However, whether NLR can effectors from multiple species has rarely investigated. Here, we identified a new RXLR-WY effector AVRamr3 P. is recognized by Rpi-amr3 wild Solanaceae Solanum americanum. associates with planta. broadly conserved different species, recognition homologs activates resistance pathogens, including tobacco black shank cacao pod pathogens parasitica palmivora. thus first characterized gene acts or These findings suggest novel path redeploy known R important pathogens.

Language: Английский

Citations

49

Cell-type-specific responses to fungal infection in plants revealed by single-cell transcriptomics DOI Creative Commons
Bozeng Tang, Feng Li, Michelle T. Hulin

et al.

Cell Host & Microbe, Journal Year: 2023, Volume and Issue: 31(10), P. 1732 - 1747.e5

Published: Sept. 22, 2023

Pathogen infection is a dynamic process. Here, we employ single-cell transcriptomics to investigate plant response heterogeneity. By generating an Arabidopsis thaliana leaf atlas encompassing 95,040 cells during by fungal pathogen, Colletotrichum higginsianum, unveil cell-type-specific gene expression, notably enrichment of intracellular immune receptors in vasculature cells. Trajectory inference identifies that had different interactions with the invading fungus. This analysis divulges transcriptional reprogramming abscisic acid signaling specifically occurring guard cells, which consistent stomatal closure dependent on direct contact Furthermore, plasticity genes involved glucosinolate biosynthesis at sites, emphasizing contribution epidermis-expressed MYB122 disease resistance. work underscores spatially dynamic, responses pathogen and provides valuable resource supports in-depth investigations plant-pathogen interactions.

Language: Английский

Citations

44

Show me your ID: NLR immune receptors with integrated domains in plants DOI Creative Commons
Clémence Marchal, Vassiliki A. Michalopoulou, Zhou Zou

et al.

Essays in Biochemistry, Journal Year: 2022, Volume and Issue: 66(5), P. 527 - 539

Published: June 6, 2022

Nucleotide-binding and leucine-rich repeat receptors (NLRs) are intracellular plant immune that recognize pathogen effectors secreted into the cell. Canonical NLRs typically contain three conserved domains including a central nucleotide binding (NB-ARC) domain, C-terminal repeats (LRRs) an N-terminal domain. A subfamily of additional noncanonical domain(s) have potentially evolved from integration effector targets in canonical NLR structure. These with extra thus referred to as integrated (NLR-IDs). Here, we first summarize our current understanding NLR-ID activation upon binding, focusing on pairs Pik-1/Pik-2, RGA4/RGA5, RRS1/RPS4. We speculate their potential oligomerization resistosomes it was recently shown for certain NLRs. Furthermore, discuss how growing mode action continuously informs engineering approaches design new resistance specificities context rapidly evolving pathogens.

Language: Английский

Citations

40

Resurrection of plant disease resistance proteins via helper NLR bioengineering DOI Creative Commons
Mauricio P. Contreras, Hsuan Pai, Muniyandi Selvaraj

et al.

Science Advances, Journal Year: 2023, Volume and Issue: 9(18)

Published: May 3, 2023

Parasites counteract host immunity by suppressing helper nucleotide binding and leucine-rich repeat (NLR) proteins that function as central nodes in immune receptor networks. Understanding the mechanisms of immunosuppression can lead to strategies for bioengineering disease resistance. Here, we show a cyst nematode virulence effector binds inhibits oligomerization NLR protein NRC2 physically preventing intramolecular rearrangements required activation. An amino acid polymorphism at interface between inhibitor is sufficient this evade suppression, thereby restoring activity multiple resistance genes. This points potential strategy resurrecting crop genomes.

Language: Английский

Citations

40

Jurassic NLR: Conserved and dynamic evolutionary features of the atypically ancient immune receptor ZAR1 DOI
Hiroaki Adachi, Toshiyuki Sakai, Jiorgos Kourelis

et al.

The Plant Cell, Journal Year: 2023, Volume and Issue: 35(10), P. 3662 - 3685

Published: July 19, 2023

Abstract Plant nucleotide-binding leucine-rich repeat (NLR) immune receptors generally exhibit hallmarks of rapid evolution, even at the intraspecific level. We used iterative sequence similarity searches coupled with phylogenetic analyses to reconstruct evolutionary history HOPZ-ACTIVATED RESISTANCE1 (ZAR1), an atypically conserved NLR that traces its origin early flowering plant lineages ∼220 150 million yrs ago (Jurassic period). discovered 120 ZAR1 orthologs in 88 species, including monocot Colocasia esculenta, magnoliid Cinnamomum micranthum, and most eudicots, notably Ranunculales species Aquilegia coerulea, which is outside core eudicots. Ortholog revealed highly features ZAR1, regions for pathogen effector recognition cell death activation. functionally reconstructed activity partner receptor-like cytoplasmic kinase (RLCK) from distantly related experimentally validating hypothesis evolved RLCKs evolution. In addition, acquired novel molecular features. cassava (Manihot esculenta) cotton (Gossypium spp.), carries a C-terminal thioredoxin-like domain, several taxa, duplicated into 2 paralog families, underwent distinct paths. stands out among angiosperm genes having experienced relatively limited duplication expansion throughout deep history. Nonetheless, also gave rise noncanonical NLRs integrated domains degenerated

Language: Английский

Citations

33

Altering Specificity and Autoactivity of Plant Immune Receptors Sr33 and Sr50 Via a Rational Engineering Approach DOI Creative Commons
Janina Tamborski, Kyungyong Seong, Furong Liu

et al.

Molecular Plant-Microbe Interactions, Journal Year: 2023, Volume and Issue: 36(7), P. 434 - 446

Published: March 3, 2023

Many resistance genes deployed against pathogens in crops are intracellular nucleotide-binding (NB) leucine-rich repeat (LRR) receptors (NLRs). The ability to rationally engineer the specificity of NLRs will be crucial response newly emerging crop diseases. Successful attempts modify NLR recognition have been limited untargeted approaches or depended on previously available structural information knowledge pathogen-effector targets. However, this is not for most NLR-effector pairs. Here, we demonstrate precise prediction and subsequent transfer residues involved effector between two closely related without their experimentally determined structure detailed about pathogen By combining phylogenetics, allele diversity analysis, modeling, successfully predicted mediating interaction Sr50 with its cognate AvrSr50 transferred Sr33. We created synthetic versions Sr33 that contain amino acids from Sr50, including Sr33syn, which gained recognize 12 amino-acid substitutions. Furthermore, discovered sites LRR domain needed also influence autoactivity Sr50. Structural modeling suggests these interact a part NB-ARC domain, named latch, possibly maintain inactive state receptor. Our approach demonstrates rational modifications NLRs, could useful enhance existing elite germplasm. [Formula: see text] Copyright © 2023 Author(s). This an open access article distributed under CC BY-NC-ND 4.0 International license.

Language: Английский

Citations

32

Disentangling the complex gene interaction networks between rice and the blast fungus identifies a new pathogen effector DOI Creative Commons
Yu Sugihara,

Yoshiko Abe,

Hiroki Takagi

et al.

PLoS Biology, Journal Year: 2023, Volume and Issue: 21(1), P. e3001945 - e3001945

Published: Jan. 19, 2023

Studies focused solely on single organisms can fail to identify the networks underlying host-pathogen gene-for-gene interactions. Here, we integrate genetic analyses of rice (Oryza sativa, host) and blast fungus (Magnaporthe oryzae, pathogen) uncover a new pathogen recognition specificity nucleotide-binding domain leucine-rich repeat protein (NLR) immune receptor Pik, which mediates resistance M. oryzae expressing avirulence effector gene AVR-Pik. Rice Piks-1, encoded by an allele Pik-1, recognizes previously unidentified AVR-Mgk1, is found mini-chromosome. AVR-Mgk1 has no sequence similarity known AVR-Pik effectors prone deletion from mini-chromosome mediated repeated Inago2 retrotransposon sequences. detected Piks-1 other Pik-1 alleles recognize effectors; binding integrated heavy metal-associated (HMA) alleles. Our findings highlight how complex interaction be disentangled applying forward genetics approaches simultaneously host pathogen. We demonstrate dynamic coevolution between NLR multiple families proteins.

Language: Английский

Citations

30

An atypical NLR protein modulates the NRC immune receptor network in Nicotiana benthamiana DOI Creative Commons
Hiroaki Adachi, Toshiyuki Sakai, Adeline Harant

et al.

PLoS Genetics, Journal Year: 2023, Volume and Issue: 19(1), P. e1010500 - e1010500

Published: Jan. 19, 2023

The NRC immune receptor network has evolved in asterid plants from a pair of linked genes into genetically dispersed and phylogenetically structured sensor helper NLR (nucleotide-binding domain leucine-rich repeat-containing) proteins. In some species, such as the model plant Nicotiana benthamiana other Solanaceae, (NLR-REQUIRED FOR CELL DEATH) forms up to half NLRome, NRCs are scattered throughout genome gene clusters varying complexities. Here, we describe NRCX, an atypical member family that lacks canonical features these proteins, functional N-terminal MADA motif capacity trigger autoimmunity. contrast NRCs, systemic silencing NRCX N . markedly impairs growth resulting dwarf phenotype. Remarkably, dwarfism silenced is partially dependent on paralogs NRC2 NRC3, but not NRC4. Despite its negative impact when systemically, spot mature leaves doesn’t result visible cell death phenotypes. However, alteration expression modulates hypersensitive response mediated by NRC3 manner consistent with role for network. We conclude contribute homeostasis this unlinked

Language: Английский

Citations

29