Plant hormones play important roles in regulating developmental processes and signaling networks involved in plant responses to a wide range of biotic and abiotic stresses. Significant progress has been made in identifying the key components and understanding the role of salicylic acid (SA), jasmonates (JA) and ethylene (ET) in plant responses to biotic stresses. Recent studies indicate that other hormones such as abscisic acid (ABA), auxin, gibberellic acid (GA), cytokinin (CK), brassinosteroids (BR) and peptide hormones are also implicated in plant defence signaling pathways but their role in plant defence is less well studied. Here, we review recent advances made in understanding the role of these hormones in modulating plant defence responses against various diseases and pests.

Role of plant hormones in plant defence responses.

FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis.

Plants sense potential microbial invaders by using pattern-recognition receptors to recognize pathogen-associated molecular patterns (PAMPs). In Arabidopsis thaliana, the leucine-rich repeat receptor kinases flagellin-sensitive 2 (FLS2) (ref. 2) and elongation factor Tu receptor (EFR) (ref. 3) act as pattern-recognition receptors for the bacterial PAMPs flagellin and elongation factor Tu (EF-Tu) (ref. 5) and contribute to resistance against bacterial pathogens. Little is known about the molecular mechanisms that link receptor activation to intracellular signal transduction. Here we show that BAK1 (BRI1-associated receptor kinase 1), a leucine-rich repeat receptor-like kinase that has been reported to regulate the brassinosteroid receptor BRI1 (refs 6,7), is involved in signalling by FLS2 and EFR. Plants carrying bak1 mutations show normal flagellin binding but abnormal early and late flagellin-triggered responses, indicating that BAK1 acts as a positive regulator in signalling. The bak1-mutant plants also show a reduction in early, but not late, EF-Tu-triggered responses. The decrease in responses to PAMPs is not due to reduced sensitivity to brassinosteroids. We provide evidence that FLS2 and BAK1 form a complex in vivo, in a specific ligand-dependent manner, within the first minutes of stimulation with flagellin. Thus, BAK1 is not only associated with developmental regulation through the plant hormone receptor BRI1 (refs 6,7), but also has a functional role in PRR-dependent signalling, which initiates innate immunity.

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A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence

Until recently, most studies on the role of hormones in plant-pathogen interactions focused on salicylic acid (SA), jasmonic acid (JA), and ethylene (ET). It is now clear that pathogen-induced modulation of signaling via other hormones contributes to virulence. A picture is emerging of complex crosstalk and induced hormonal changes that modulate disease and resistance, with outcomes dependent on pathogen lifestyles and the genetic constitution of the host. Recent progress has revealed intriguing similarities between hormone signaling mechanisms, with gene induction responses often achieved by derepression. Here, we report on recent advances, updating current knowledge on classical defense hormones SA, JA, and ET, and the roles of auxin, abscisic acid (ABA), cytokinins (CKs), and brassinosteroids in molding plant-pathogen interactions. We highlight an emerging theme that positive and negative regulators of these disparate hormone signaling pathways are crucial regulatory targets of hormonal crosstalk in disease and defense.

Hormone Crosstalk in Plant Disease and Defense: More Than Just JASMONATE-SALICYLATE Antagonism

BAK1, an Arabidopsis LRR Receptor-like Protein Kinase, Interacts with BRI1 and Modulates Brassinosteroid Signaling

Brassinosteroid-insensitive 1 (BRI1) of Arabidopsis thaliana encodes a cell surface receptor for brassinosteroids. Mutations in BRI1 severely affect plant growth and development. Activation tagging of a weak bri1 allele (bri1-5) resulted in the identification of a new locus, brs1-1D. BRS1 is predicted to encode a secreted carboxypeptidase. Whereas a brs1 loss-of-function allele has no obvious mutant phenotype, overexpression of BRS1 can suppress bri1 extracellular domain mutants. Genetic analyses showed that brassinosteroids and a functional BRI1 protein kinase domain are required for suppression. In addition, overexpressed BRS1 missense mutants, predicted to abolish BRS1 protease activity, failed to suppress bri1-5. Finally, the effects of BRS1 are selective: overexpression in either wild-type or two other receptor kinase mutants resulted in no phenotypic alterations. These results strongly suggest that BRS1 processes a protein involved in an early event in the BRI1 signaling.

https://www.pnas.org/content/pnas/98/10/5916.full.pdf

BRS1, a serine carboxypeptidase, regulates BRI1 signaling in Arabidopsis thaliana

In the era of genomics, if a gene is not annotated, it is not investigated. Due to their small size, genes encoding peptides are often missed in genome annotations. Secreted peptides are important regulators of plant growth, development, and physiology. Identification of additional peptide signals by sequence homology searches has had limited success due to sequence heterogeneity. A bioinformatics approach was taken to find unannotated Arabidopsis (Arabidopsis thaliana) peptides. Arabidopsis chromosome sequences were searched for all open reading frames (ORFs) encoding peptides and small proteins between 25 and 250 amino acids in length. The translated ORFs were then sequentially queried for the presence of an amino-terminal cleavable signal peptide, the absence of transmembrane domains, and the absence of endoplasmic reticulum lumenal retention sequences. Next, the ORFs were filtered against the The Arabidopsis Information Resource 6.0 annotated Arabidopsis genes to remove those ORFs overlapping known genes. The remaining 33,809 ORFs were placed in a relational database to which additional annotation data were deposited. Genome-wide tiling array data were compared with the coordinates of the ORFs, supporting the possibility that many of the ORFs may be expressed. In addition, clustering and sequence similarity analyses revealed that many of the putative peptides are in gene families and/or appear to be present in the rice (Oryza sativa) genome. A subset of the ORFs was evaluated by reverse transcription-PCR and, for one-fifth of those, expression was detected. These results support the idea that the number and diversity of plant peptides is broader than currently assumed. The peptides identified and their annotation data may be viewed or downloaded through a searchable Web interface at peptidome.missouri.edu.

The Arabidopsis Unannotated Secreted Peptide Database, a Resource for Plant Peptidomics

A genetic screen was performed to find new mutants with an erecta (er) phenotype and to identify genes that may function with ER, a receptor-like kinase. These mutants were named elk (for erecta-like) and were placed into five complementation groups. We positionally cloned ELK4 and determined that it encodes AGB1, a putative heterotrimeric G-protein beta subunit. Therefore, elk4 was renamed agb1. agb1-1 plants express similar fruit phenotypes, as seen in er plants, but differ from er in that the stem is only slightly shorter than that in the wild type, the pedicel is slightly longer than that in the wild type, and the leaves are rounder than those in er mutants. Molecular analysis of agb1-1 indicates that it is likely a null allele. AGB1 mRNA is expressed in all tissues tested but is highest in the silique. Analysis of agb1-1 er double mutants suggests that AGB1 may function in an ER developmental pathway regulating silique width but that it functions in parallel pathways affecting silique length as well as leaf and stem development. The finding that AGB1 is involved in the control of organ shape suggests that heterotrimeric G-protein signaling is a developmental regulator in Arabidopsis.

A Mutant Arabidopsis Heterotrimeric G-Protein β Subunit Affects Leaf, Flower, and Fruit Development

Small polypeptides can act as important regulatory molecules that coordinate cellular responses required for differentiation, growth, and development. In a gain-of-function genetic screen for genes that influence fruit development in Arabidopsis, we identified a novel gene - DEVIL1 (DVL1) - encoding a small protein. Overexpression of DVL1 results in pleiotropic phenotypes featured by shortened stature, rounder rosette leaves, clustered inflorescences, shortened pedicles, and siliques with pronged tips. cDNA analysis indicates that DVL1 has a 153-nucleotide (nt) open-reading frame (ORF) encoding a 51-amino acid polypeptide that shares no significant similarity to previously identified proteins. Sequence alignment shows that DVL1 belongs to a family of related genes that are limited to angiosperm plants. Ectopic overexpression of each of the five closely related Arabidopsis DVL genes causes similar phenotypic changes, suggesting overlapping function in the DVL gene family. Point mutations of conserved amino acids in the C-terminal region of the DVL1 polypeptide reveal that these conserved residues are required for DVL1-overexpression phenotypes. Our results show that the DVL family is a novel class of small polypeptides and the overexpression phenotypes suggest that these polypeptides may have a role in plant development.

https://onlinelibrary.wiley.com/doi/pdf/10.1111/j.1365-313X.2003.01994.x

Kevin A. Lease

Papers

BAK1, an Arabidopsis LRR Receptor-like Protein Kinase, Interacts with BRI1 and Modulates Brassinosteroid Signaling

BRS1, a serine carboxypeptidase, regulates BRI1 signaling in Arabidopsis thaliana

The Arabidopsis Unannotated Secreted Peptide Database, a Resource for Plant Peptidomics

A Mutant Arabidopsis Heterotrimeric G-Protein β Subunit Affects Leaf, Flower, and Fruit Development

DVL, a novel class of small polypeptides: overexpression alters Arabidopsis development.