Evolution of herbivore-induced early defense signaling was shaped by genome-wide duplications in Nicotiana

Autor: Ian T. Baldwin, Shuqing Xu, Zhihao Ling, Wenwu Zhou, Ashton Omdahl, Thomas Brockmöller
Rok vydání: 2016
Předmět:
0106 biological sciences
0301 basic medicine
Plant Biology
01 natural sciences
Genome
chemistry.chemical_compound
Gene Expression Regulation
Plant

Gene Duplication
Plant defense against herbivory
Plant Immunity
herbivore-induced defense
Biology (General)
Organism
Genetics
biology
General Neuroscience
Jasmonic acid
food and beverages
General Medicine
Genomics and Evolutionary Biology
Medicine
Plant hormone
transposable elements
Genome
Plant

Research Article
Signal Transduction
Nicotiana
QH301-705.5
Science
Cyclopentanes
General Biochemistry
Genetics and Molecular Biology

Evolution
Molecular

03 medical and health sciences
Tobacco
genome duplication
Botany
Herbivory
Oxylipins
Gene
General Immunology and Microbiology
Gene Expression Profiling
jasmonic acid
fungi
biology.organism_classification
030104 developmental biology
chemistry
Other
010606 plant biology & botany
Zdroj: eLife, Vol 5 (2016)
eLife
ISSN: 2050-084X
Popis: Herbivore-induced defenses are widespread, rapidly evolving and relevant for plant fitness. Such induced defenses are often mediated by early defense signaling (EDS) rapidly activated by the perception of herbivore associated elicitors (HAE) that includes transient accumulations of jasmonic acid (JA). Analyzing 60 HAE-induced leaf transcriptomes from closely-related Nicotiana species revealed a key gene co-expression network (M4 module) which is co-activated with the HAE-induced JA accumulations but is elicited independently of JA, as revealed in plants silenced in JA signaling. Functional annotations of the M4 module were consistent with roles in EDS and a newly identified hub gene of the M4 module (NaLRRK1) mediates a negative feedback loop with JA signaling. Phylogenomic analysis revealed preferential gene retention after genome-wide duplications shaped the evolution of HAE-induced EDS in Nicotiana. These results highlight the importance of genome-wide duplications in the evolution of adaptive traits in plants. DOI: http://dx.doi.org/10.7554/eLife.19531.001
eLife digest A variety of different insects feed on plants and these insects often produce molecules known as elicitors that the plants can recognize. This triggers a sophisticated suite of defenses in the plant that can either deter feeding by the insects, or help the plants endure the attack. The elicitors stimulate the rapid accumulation of a plant hormone called jasmonic acid, which in turn activates the defense responses. However, high levels of jasmonic acid can also reduce the ability of the plants to survive and reproduce by activating plant defenses when they are not needed. Therefore, plants need to regulate the signaling networks that control defense so that jasmonic acid only accumulates when the benefit of fighting the insect outweighs the cost of producing the defenses. The costs and benefits of defense responses vary among different insects and environmental conditions, which has made it difficult to study how plants regulate defense signaling networks. To address this question, Zhou et al. investigated the activities of genes in six species of tobacco plant after they have been exposed to different insect elicitors. The experiments identified a network of genes that is activated in response to elicitors and acts largely independent of jasmonic acid signaling. A newly identified gene in this network called NaLRRK1 and jasmonic acid suppress each other, suggesting that NaLRRK1 helps to regulate jasmonic acid levels. Further analysis shows that a process called genome duplication, in which all the genes in an organism are copied, has shaped the evolution of early defense signaling in Nicotiana. Many of the duplicated genes have adopted new roles and been retained in the plants. This highlights the importance of genome duplications in helping plants to adapt to their environment. The next challenge following on from this work would be to identify what specific roles these genes play in the plants, and how they affect the ability of plants to survive insect attacks in their native habitats. DOI: http://dx.doi.org/10.7554/eLife.19531.002
Databáze: OpenAIRE