Cell Wall Formation Pathways Are Differentially Regulated in Sugarcane Contrasting Genotypes Associated with Endophytic Diazotrophic Bacteria

Overview

Journal Planta

Specialty Biology

Date 2021 Oct 27

PMID 34705112

Citations 5

Authors

Helkin Giovani F Ballesteros

Aline C Rosman

Thais Louise G Carvalho

Clicia Grativol

Adriana Silva Hemerly

Affiliations

Soon will be listed here.

Abstract

Differences in cell wall components between two BNF-contrasting sugarcane genotypes might result from genetic variations particular to the genotype and from the efficiency in diazotrophic bacteria association. Sugarcane is a plant of the grass family (Poaceae) that is highly cultivated in Brazil, as an important energy resource. Commercial sugarcane genotypes may be successfully associated with beneficial endophytic nitrogen-fixing bacteria, which can influence several plant metabolic pathways, such as cell division and growth, synthesis of hormones, and defense compounds. In this study, we investigated how diazotrophic bacteria associated with sugarcane plants could be involved in the regulation of cell wall formation pathways. A molecular and structural characterization of the cell wall was compared between two genotypes of sugarcane with contrasting rates of Biological Nitrogen Fixation (BNF): SP70-1143 (high BNF) and Chunee (low BNF). Differentially expressed transcripts were identified in transcriptomes generated from SP70-1143 and Chunee. Expression profiles of cellulose and lignin genes, which were more expressed in SP70-1134, and callose genes, which were more expressed in Chunee, were validated by RT-qPCR and microscopic analysis of cell wall components in tissue sections. A similar expression profile in both BNF-contrasting genotypes was observed in naturally colonized plants and in plants inoculated with G. diazotrophicus. Cell walls of the high BNF genotype have a greater cellulose content, which might contribute to increase biomass. In parallel, callose was concentrated in the vascular tissues of the low BNF genotype and could possibly represent a barrier for an efficient bacterial colonization and dissemination in sugarcane tissues. Our data show a correlation between the gene profiles identified in the BNF-contrasting genotypes and a successful association with endophytic diazotrophic bacteria.

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References

Bidhendi A, Chebli Y, Geitmann A . Fluorescence visualization of cellulose and pectin in the primary plant cell wall. J Microsc. 2020; 278(3):164-181. DOI: 10.1111/jmi.12895. View

Bottcher A, Cesarino I, Dos Santos A, Vicentini R, Mayer J, Vanholme R . Lignification in sugarcane: biochemical characterization, gene discovery, and expression analysis in two genotypes contrasting for lignin content. Plant Physiol. 2013; 163(4):1539-57. PMC: 3850185. DOI: 10.1104/pp.113.225250. View

Carroll A, Mansoori N, Li S, Lei L, Vernhettes S, Visser R . Complexes with mixed primary and secondary cellulose synthases are functional in Arabidopsis plants. Plant Physiol. 2012; 160(2):726-37. PMC: 3461551. DOI: 10.1104/pp.112.199208. View

Carvalho T, Balsemao-Pires E, Saraiva R, Ferreira P, Hemerly A . Nitrogen signalling in plant interactions with associative and endophytic diazotrophic bacteria. J Exp Bot. 2014; 65(19):5631-42. DOI: 10.1093/jxb/eru319. View

Carvalho T, Ballesteros H, Thiebaut F, Ferreira P, Hemerly A . Nice to meet you: genetic, epigenetic and metabolic controls of plant perception of beneficial associative and endophytic diazotrophic bacteria in non-leguminous plants. Plant Mol Biol. 2016; 90(6):561-74. DOI: 10.1007/s11103-016-0435-1. View

Chapelle A, Morreel K, Vanholme R, Le-Bris P, Morin H, Lapierre C . Impact of the absence of stem-specific β-glucosidases on lignin and monolignols. Plant Physiol. 2012; 160(3):1204-17. PMC: 3490608. DOI: 10.1104/pp.112.203364. View

Chen X, Kim J . Callose synthesis in higher plants. Plant Signal Behav. 2009; 4(6):489-92. PMC: 2688293. DOI: 10.4161/psb.4.6.8359. View

Chen X, Marszalkowska M, Reinhold-Hurek B . Jasmonic Acid, Not Salicyclic Acid Restricts Endophytic Root Colonization of Rice. Front Plant Sci. 2020; 10:1758. PMC: 7000620. DOI: 10.3389/fpls.2019.01758. View

Cho H, Cosgrove D . Altered expression of expansin modulates leaf growth and pedicel abscission in Arabidopsis thaliana. Proc Natl Acad Sci U S A. 2000; 97(17):9783-8. PMC: 16942. DOI: 10.1073/pnas.160276997. View

10.

Correr F, Hosaka G, Gomez S, Cia M, Monteiro Vitorello C, Camargo L . Time-series expression profiling of sugarcane leaves infected with Puccinia kuehnii reveals an ineffective defense system leading to susceptibility. Plant Cell Rep. 2020; 39(7):873-889. DOI: 10.1007/s00299-020-02536-w. View

11.

De Lorenzo G, Ferrari S, Giovannoni M, Mattei B, Cervone F . Cell wall traits that influence plant development, immunity, and bioconversion. Plant J. 2018; 97(1):134-147. DOI: 10.1111/tpj.14196. View

12.

Deng Y, Chen H, Li C, Xu J, Qi Q, Xu Y . Endophyte evade plant defense by producing lantibiotic subtilomycin to mask self-produced flagellin. Commun Biol. 2019; 2:368. PMC: 6787100. DOI: 10.1038/s42003-019-0614-0. View

13.

Donaldson L, Kroese H, Hill S, Franich R . Detection of wood cell wall porosity using small carbohydrate molecules and confocal fluorescence microscopy. J Microsc. 2015; 259(3):228-36. DOI: 10.1111/jmi.12257. View

14.

Dong X, Hong Z, Chatterjee J, Kim S, Verma D . Expression of callose synthase genes and its connection with Npr1 signaling pathway during pathogen infection. Planta. 2008; 229(1):87-98. DOI: 10.1007/s00425-008-0812-3. View

15.

Engelsdorf T, Gigli-Bisceglia N, Veerabagu M, McKenna J, Vaahtera L, Augstein F . The plant cell wall integrity maintenance and immune signaling systems cooperate to control stress responses in . Sci Signal. 2018; 11(536). DOI: 10.1126/scisignal.aao3070. View

16.

Fagard M, Desnos T, Desprez T, Goubet F, Refregier G, Mouille G . PROCUSTE1 encodes a cellulose synthase required for normal cell elongation specifically in roots and dark-grown hypocotyls of Arabidopsis. Plant Cell. 2001; 12(12):2409-2424. PMC: 102227. DOI: 10.1105/tpc.12.12.2409. View

17.

Ferreira S, Hotta C, Poelking V, Leite D, Buckeridge M, Ehlers Loureiro M . Co-expression network analysis reveals transcription factors associated to cell wall biosynthesis in sugarcane. Plant Mol Biol. 2016; 91(1-2):15-35. PMC: 4837222. DOI: 10.1007/s11103-016-0434-2. View

18.

Gallego-Giraldo L, Pose S, Pattathil S, Peralta A, Hahn M, Ayre B . Elicitors and defense gene induction in plants with altered lignin compositions. New Phytol. 2018; 219(4):1235-1251. DOI: 10.1111/nph.15258. View

19.

Hardoim P, van Overbeek L, van Elsas J . Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol. 2008; 16(10):463-71. DOI: 10.1016/j.tim.2008.07.008. View

20.

Hofte H, Voxeur A . Plant cell walls. Curr Biol. 2017; 27(17):R865-R870. DOI: 10.1016/j.cub.2017.05.025. View