Genetic diversity and plant-plant interactions as drivers of disease resistance in cereals

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Genetic diversity and plant-plant interactions as

drivers of disease resistance in cereals

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2 Water nutrients microbiota microbiota neighbors Signal integration Plant health

Ballini et al, RICE 2013

Huang et al, Frontiers in Plant Science 2017 Bidzinski et al,

Frontiers in Plant Science 2016

Defense stimulators

Subrahmaniam et al, Plant 2018 Zhu and Morel, MPMI 2019

Henry et al, Plant Sign Behav 2020 Alonso et al,

Env Microb 2020

Ballini et al, Euphytica 2020

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3 Plant-soil feedbacks and legacies Stranger recognition Competition Kin recognition Danger signalization Microbiota modification Constitutive VOCs loliolide, allantoin allelochemicals SAS Root density, nutrient foraging Root exudates Root Exudates, small peptides Inducible VOCs

Markovic et al, JEBX. 2019 Wenig et al, Nature com. 2019 Orlovskis et al, New phytol. 2020 Coppola et al, Scientific reports. 2017

Biedrzycki et al, Plant Signaling & Behavior 2011

Wit et al, Plant Journal 2013 Cerrudo et al, Plant Physiology 2012 Ballaré, An. rev. of Plant biology 2014 Chen et al. Frontiers in P. Science, 2019

Sukegawa et al. Plant journal, 2018 Venturelli et al. Plant cell, 2015 Kong et al. 2018 Li et al. JEBX, 2020 Murata et al, Plant phisiology 2019 Takagi et al. JEBX, 2016 Cheng et al. Scientific report, 2016

Ma et al, Frontier in plant science. 2017 Beredsen et al, ISME journal. 2018 Yuan et al, Microbiome. 2018 Hu et al, Nature com. 2018 Wang et al. New phytol, 2019

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Intraspecific competition for nutrients between conspecifics

Intraspecific competition

Intraspecific plant density

SAS

Competition for nutrient

Shade Avoidance Syndrom increases A.thaliana susceptibility

to pathogens

Root interaction with conspecifics increases accumulation of chemical

defense in tobacco

Wit et al, Plant Journal 2013 Cerrudo et al, Plant Physiology 2012 Review in Ballaré, An. rev. of Plant biology 2014

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Stranger’s things from healthy neighbors

Allelochemicals Constitutive VOCs Menthol (cVOCs) Modifiying histone acetylation of promoters of defense genes DIMBOA and derivatives (-)-Loliolide Allantoine Diallyl disulfide - Defense gene upregulated - Herbivory & pathogen resistance increased - Production of allelopathic molecules against parasites

Sukegawa et al. Plant journal, 2018

Venturelli et al. Plant cell, 2015 Kong et al. 2018

Li et al. JEBX, 2020 Murata et al, Plant phisiology 2019

Takagi et al. JEBX, 2016

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DIMBOA?

(Venturelli et al, 2015) DIMBOA

RESISTANCE

DIMBOA

derivatives HDAC defense

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0 10 20 30 40

Rice Rice + Maize

average lesions/ rice leaf

*

(Nipponbare and B73) Rice blast disease

(GY11) 0 0,5 1 1,5 2 2,5 Maize Maize+Rice normalized average lesions/maize leaf ** (B73 and Maratelli) Maize blast disease

(2 isolates)

~40% reduction of symptoms

Intercropping rice and maize

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0 0,5 1 1,5 2 2,5 rice W22 bx1 (W22) B73 bx1 (B73) D isease lev el (n o rmal iz ed ) * *

DIMBOA biosynthesis is required for protection in intercropping

focal neighbor

rice

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Plants leave a message : plant soil feedback and legacies

Wikipedia

Plant–soil feedback is a process where plants alter the biotic and abiotic qualities of soil they grow in, which then alters the ability of plants to grow in that soil in the future

Microbiota modification

Intraspecific & Interspecific

Inductible or constitutive

Induces defense genes, pathogen and herbivory resistance

Depend on specific species of fungi, bacteria or combinaison

Wang et al. New phytol, 2019 Hu et al, Nature com. 2018 Beredsen et al, ISME journal. 2018

Yuan et al, Microbiome. 2018 Ma et al, Frontier in plant science. 2017

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The neighbor watch, Signalisation of danger between plant

Disease / attack plant

iVOCs, HIPV etc

..

Inductible Root exudates, small peptides ...

Systemin Excreted soil peptide

(18 AA) by tomato roots Monoterpene Propagation of SAR (Systemic acquired Resistance) between neighbor plants Unknown root signal

Inducible VOCs Can be triggered by touch in maize

Coppola et al, Scientific reports. 2017 Orlovskis et al, New phytol. 2020 Wenig et al, Nature com. 2019

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Plants modulate immunity and susceptiblity in their neighborhood

Pelissier, Violle and Morel, review submitted

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Kin recognition: when plants recognize conspecifics

O= Own= plant alone K= Kin= 2 plants together

S= Stranger= different ecotype Biedrzycki et al, Plant Signaling & Behavior 2011

Only one example to our knowledge shows that Kin recognition can trigger the expression of immunity (kin relations known to affect response to insects)

Kin recognition is an organism's ability to distinguish between close genetic kin and non-kin Wikipedia

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Pure

A

B

C

D

Mix ₁₆

Screening for Neighbor-modulated susceptiblity

Specific ability of a given neighbor

to modulate

susceptibility of focal A (« good » or « bad » neighbor)

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B las t susc eptib ili ty

Neighbor-modulated susceptibility (NMS) in rice and wheat

Le af rus t suscep tibl ity

Pelissier et al, submitted

Magnaporthe oryzae Puccinia triticina

WHEAT

RICE

Some kins can modulate susceptiblity in their neighborhood (NMS)

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NMS takes place in the soil and does not require microbiome (nor an infected neighbor)

Localization of intra-specific plant-plant interactions leading to NMS

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Pelissier et al, submitted

Bla st su scep tib ility Le af rus t suscep tibl ity WHEAT RICE

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Focal plant = Kitaake CO-CULTURE Neighbor plant = 280 genotypes of temperate japonica Blast susceptibility on Kitaake X 3 replicates GWAS

(Genome Wide Association Study) of NMS emission 19

.

Mapping rice ability to modulate susceptibility in its neighborhood

Pelissier et al, unpublished

Rémi

Diversity of NMS?

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Neighbors can reduce but also increase disease susceptibilty of Kitaake

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Blast susceptibility of Kitaake cultivated with 280 differents neighbors

Les ion nu mbe r/ lea f su rf ace X 2,3 X 1/7 280 rice neighbors

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GWAS of the emission of NMS

LD block= 250kb 9 coding sequences, incl. 6 genes

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***

Test of GWAS prediction for emission of NMS

*

Neighbor haplotype Ki taak e su scep ti bil ity Independent validation (6 haplotype 3 vs 6 haplotypes 1 or 2) Susceptibility data from GWAS

GWAS predicts that neighbors with haplotype 3 reduce susceptiblity in focal kitaake

Ki taak e sus cep ti bil ity Neighbor haplotype 20% reduction of susceptibility

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NMS at the species level: the case of temperate japonica rice

Temperate japonica rice

Nipponbare Baldo Calmochi Gritna Lido Lomellino Luxor M204 Maratelli OTA Sesia Kitaake Ba ld o Ca lm oc h i Gr itn a Li d o Lome lli n o Lu xor M 20 4 M ar at e lli O TA Se si a Ni p p on b ar e K it aa ke Foc al pl an t Neighbor plant 23 More R More S + 14 % Rice Blast fungus

Sus cep ti bil ity ( norm .)

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Cultivated durum wheat * * * * * * * * * * * * * * * *

Wheat X leaf rust

* _** * * * ** _* * . . . _** Acuce rice EPO Wheat * * * * * Japonica Rice * _* _* _* * * * *

NMS: good neighbor and good focal plants

Rice X Blast fungus

More R More S Pelissier et al, unpublished

Foc al pl an t Neighbor plant

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+ 27 % - 15 % + 14 % - 8 % Historical within-field co-existence

NMS and breeding

Pa thog en su scep ti bil ity Wheat (leaf rust) Rice (Blast fungus)

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Rémi Pélissier Elsa Ballini Luis Buendia Aurélie Ducasse Andy Brousse Huichuan Huang Jingjing Liao Baihui Jin Xiahong He Chenyung Li Youyong Zhu jean-benoit.morel@inrae.fr

Yunnan Agricultural University

Funding French ANR INRAE Crop protection CASDAR

International joint Lab PLANTOMIX

Cyrille Violle

Hélène Fréville

QUESTIONS?

+ projet thèse (Inrae-ANR Mobidiv)

Génétique et physiologie des interactions blé-blé modulant la sensibilité aux agents pathogènes (Sept 2021-2024)