Genome of the most noxious weed water hyacinth (Eichhornia crassipes) provides insights into plant invasiveness and its translational potential

Abstract

The invasive character of Eichhornia crassipes (water hyacinth) is a major threat to global biodiversity and ecosystems. To investigate the genomic basis of invasiveness, we performed the genome and transcriptome sequencing of E. crassipes and reported the genome of 1.11 Gbp size with 63,299 coding genes and N50 of 1.98 Mb. We confirmed a recent whole genome duplication event in E. crassipes that resulted in high intraspecific collinearity and significant expansion in gene families. Further, the orthologs gene clustering analysis and comparative evolutionary analysis with 14 other aquatic invasive and non-invasive angiosperm species revealed adaptive evolution in genes associated with plant-pathogen interaction, hormone signaling, abiotic stress tolerance, heavy metals sequestration, photosynthesis, and cell wall biosynthesis with highly expanded gene families, which contributes toward invasive characteristics of the water hyacinth. However, these characteristics also make water hyacinth an excellent candidate for biofuel production, phytoremediation, and other translational applications.

Keywords: Genomics; Plant Genetics; Plant biology.

Graphical abstract

Figure 1

E. crassipes evolutionary history (A) Morphology of E. crassipes (water hyacinth). (B) Phylogenetic tree with gene family evolution, teal bars denote the confidence intervals for estimated divergence times at each internal node. Calibrated nodes are highlighted with red dots. MRCA—most recent common ancestor. (C) Synonymous substitution rate (Ks) distributions of paralogs and orthologs of E. crassipes, E. paniculata, and M. acuminata. (D) Timing of whole-genome duplications, boxes indicate WGD events. Blue boxes indicate WGD events analyzed in this paper. (E) Stacked columns chart showing the number of gene duplications in various duplicated types and gene duplication-induced highly expanded gene numbers, PD; proximal duplication, TD; tandem duplication, DD; dispersed duplication, SD; segmental duplication. (F) KEGG enrichment of genes overlapping between highly expanded gene families and types of gene duplications.

Figure 2

Evolutionary signatures in plant-pathogen interaction PTI; pattern-triggered immunity, ETI; effector-triggered immunity, PRRs; pattern recognition receptors, PAMPs; pathogen-associated molecular patterns, elf18; elongation factor Tu, flg22; flagellin, elf18; elongation factor 18, RBOH; respiratory burst oxidase homologs, CNGC; cyclic nucleotide-gated channel, CDPK; calcium-dependent protein kinases, CaM/CML; calmodulin (CaM) and calmodulin-like (CML), NOS; nitric oxide synthase, NO; nitric oxide, MEKK1; mitogen-activated protein kinase kinase kinase, MKK1/2/4/5; mitogen-activated protein kinase 1/2/4/5, MPK3/6; mitogen-activated protein kinase 3/6, MPK4; mitogen-activated protein kinase 4, FRK1; flg22-induced receptor-like kinase 1, NHO1; nonhost 1, PR1; pathogen-related 1, RIN; RPM1-interacting protein, RPM1; resistance to pseudomonas syringae pv maculicola 1, RPS; resistance to pseudomonas syringae protein 2, PBS1; AVRPPHB SUSCEPTIBLE1, HSP90; heat shock protein 90, SGT1; suppressor of G2 allele of skp1, RAR1; required forMla12 resistance, KCS1/10; 3-ketoacyl-CoA synthase 1/10, HCD1; 3-hydroxyacyl-coA dehydratase 1, PIK1; phosphatidylinositol 4-kinase 1, AvR; avirulence, P; phosphorylation; Ub; Ubiquitination, ?; Receptors are not characterized (created with BioRender.com).

Figure 3

Evolutionary signatures in plant-hormone signaling pathways PYR/PYL; pyrabactin resistance/PYR-like, PP2C; plant protein phosphatase 2C, SnRK2; serine/threonine protein kinase, ABF; ABRE binding factors, NPR1; nonexpresser of pathogen-related genes 1, TGA; TGACG sequence specific binding transcription factors, PR-1; pathogen related 1, CRE1; cytokinin response 1, AHP; arabidopsis histidine phosphotransfer proteins, B-ARR; type-B arabidopsis response regulator, BRI1; brassinosteroid insensitive 1, BAK; brassinosteroid insensitive 1-associated receptor kinase 1, BSK; brassinosteroid signaling kinase, BKI1; BRI1 kinase inhibitor 1, BSU1; BRI1 suppressor 1, BIN2; brassinosteroid insensitive 2, BZR1/2; brassinosteroid resistant 1/2, CYCD3; cyclin D3, GID1; gibberellin insensitive dwarf 1, GID2; gibberellin insensitive dwarf 2, TF; transcription factors, AUX1; auxin influx transporter, TIR1; transport inhibitor response 1, AUX/IAA; auxin/indole-3-acetic acid, ARF; auxin response factor, GH3; auxin-responsive Gretchen Hagen3, SAUR; small auxin upregulated RNA, JAR1; jasmonate resistant 1, JA-Ile; jasmonyl-L-isoleucine, COI1; coronatine-insensitive 1, JAZ; jasmonate ZIM-domain, MYC2; myelocytomatosis 2, ETR; ethylene receptor, CTR1; constitutive triple response, MPK6; mitogen-activated protein kinase 6, EIN2; ethylene insensitive 2, EIN3; ethylene insensitive 3, EBF1/2; EIN3-binding factor 1/2, ERF1/2; ethylene response factor 1/2, P; phosphorylation; Ub; Ubiquitination (created with BioRender.com).

Figure 4

Schematic representation of C3 (Calvin-Benson) pathway showing evolutionary signatures Rubisco; ribulose bisphosphate carboxylase oxygenase, PGK; phosphoglycerate kinase, GAPDH; glyceraldehyde 3-phosphate dehydrogenase, FBPA; fructose-1,6-bisphosphate aldolase, FBPase; fructose-1,6-bisphosphatases, TK; transketolase, TPI; triosephosphate isomerase, SBPase; sedoheptulose-1,7-bisphosphatase, RPE; ribulose-phosphate 3-epimerase, RPI; ribose 5-phosphate isomerase A, PRK; phosphoribulokinase (created with BioRender.com).