Sequestration of Plant Defense Compounds by Insects: From Mechanisms to Insect–Plant Coevolution

Plant defense compounds play a key role in the evolution of insect–plant associations by selecting for behavioral, morphological, and physiological insect adaptations. Sequestration, the ability of herbivorous insects to accumulate plant defense compounds to gain a fitness advantage, represents a complex syndrome of adaptations that has evolved in all major lineages of herbivorous insects and involves various classes of plant defense compounds. In this article, we review progress in understanding how insects selectively accumulate plant defense metabolites and how the evolution of specific resistance mechanisms to these defense compounds enables sequestration. These mechanistic considerations are further integrated into the concept of insect–plant coevolution. Comparative genome and transcriptome analyses, combined with approaches based on analytical chemistry that are centered in phylogenetic frameworks, will help to reveal adaptations underlying the sequestration syndrome, which is essential to understanding the influence of sequestration on insect–plant coevolution.

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Sugar transporters enable a leaf beetle to accumulate plant defense compounds

10.1101/2021.03.03.433712 ◽

2021 ◽

Author(s):

Zhi-Ling Yang ◽

Hussam Hassan Nour-Eldin ◽

Sabine Hänniger ◽

Michael Reichelt ◽

Christoph Crocoll ◽

...

Keyword(s):

Plant Defense ◽

Flea Beetle ◽

Malpighian Tubule ◽

Transport Processes ◽

The Body ◽

Malpighian Tubules ◽

Major Facilitator Superfamily ◽

Herbivorous Insects ◽

Specialist Herbivore ◽

Defense Compounds

AbstractMany herbivorous insects selectively accumulate plant toxins for defense against predators; however, little is known about the transport processes that enable insects to absorb and store defense compounds in the body. Here, we investigate how a specialist herbivore, the horseradish flea beetle, accumulates high amounts of glucosinolate defense compounds in the hemolymph. Using phylogenetic analyses of coleopteran membrane transporters of the major facilitator superfamily, we identified a clade of glucosinolate-specific transporters (PaGTRs) belonging to the sugar porter family.PaGTRexpression was predominantly detected in the excretory system, the Malpighian tubules. Silencing ofPaGTRs led to elevated glucosinolate excretion, significantly reducing the levels of sequestered glucosinolates in beetles. This suggests thatPaGTRs reabsorb glucosinolates from the Malpighian tubule lumen to prevent their loss by excretion. Ramsay assays performed with dissected Malpighian tubules confirmed a selective retention of glucosinolates. Thus, the selective accumulation of plant defense compounds in herbivorous insects can depend on the ability to prevent excretion.

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Sugar transporters enable a leaf beetle to accumulate plant defense compounds

Nature Communications ◽

10.1038/s41467-021-22982-8 ◽

2021 ◽

Vol 12 (1) ◽

Author(s):

Zhi-Ling Yang ◽

Hussam Hassan Nour-Eldin ◽

Sabine Hänniger ◽

Michael Reichelt ◽

Christoph Crocoll ◽

...

Keyword(s):

Plant Defense ◽

Flea Beetle ◽

Malpighian Tubule ◽

Transport Processes ◽

The Body ◽

Malpighian Tubules ◽

Major Facilitator Superfamily ◽

Herbivorous Insects ◽

Specialist Herbivore ◽

Defense Compounds

AbstractMany herbivorous insects selectively accumulate plant toxins for defense against predators; however, little is known about the transport processes that enable insects to absorb and store defense compounds in the body. Here, we investigate how a specialist herbivore, the horseradish flea beetle, accumulates glucosinolate defense compounds from Brassicaceae in the hemolymph. Using phylogenetic analyses of coleopteran major facilitator superfamily transporters, we identify a clade of glucosinolate-specific transporters (PaGTRs) belonging to the sugar porter family. PaGTRs are predominantly expressed in the excretory system, the Malpighian tubules. Silencing of PaGTRs leads to elevated glucosinolate excretion, significantly reducing the levels of sequestered glucosinolates in beetles. This suggests that PaGTRs reabsorb glucosinolates from the Malpighian tubule lumen to prevent their loss by excretion. Ramsay assays corroborated the selective retention of glucosinolates by Malpighian tubules of P. armoraciae in situ. Thus, the selective accumulation of plant defense compounds in herbivorous insects can depend on the ability to prevent excretion.

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Cancer, Retrogenes, and Evolution

Life ◽

10.3390/life11010072 ◽

2021 ◽

Vol 11 (1) ◽

pp. 72

Author(s):

Klaudia Staszak ◽

Izabela Makałowska

Keyword(s):

Specific Resistance ◽

Neoplastic Transformation ◽

Resistance Mechanisms ◽

Response To Therapy ◽

Additional Gene ◽

Cancer Subtypes ◽

Gene Copies ◽

Specific Cancer ◽

Evolution Of Genomes

This review summarizes the knowledge about retrogenes in the context of cancer and evolution. The retroposition, in which the processed mRNA from parental genes undergoes reverse transcription and the resulting cDNA is integrated back into the genome, results in additional copies of existing genes. Despite the initial misconception, retroposition-derived copies can become functional, and due to their role in the molecular evolution of genomes, they have been named the “seeds of evolution”. It is convincing that retrogenes, as important elements involved in the evolution of species, also take part in the evolution of neoplastic tumors at the cell and species levels. The occurrence of specific “resistance mechanisms” to neoplastic transformation in some species has been noted. This phenomenon has been related to additional gene copies, including retrogenes. In addition, the role of retrogenes in the evolution of tumors has been described. Retrogene expression correlates with the occurrence of specific cancer subtypes, their stages, and their response to therapy. Phylogenetic insights into retrogenes show that most cancer-related retrocopies arose in the lineage of primates, and the number of identified cancer-related retrogenes demonstrates that these duplicates are quite important players in human carcinogenesis.

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Identification of Race-Specific Resistance in North American Vitis spp. Limiting Erysiphe necator Hyphal Growth

Phytopathology ◽

10.1094/phyto-03-11-0062 ◽

2012 ◽

Vol 102 (1) ◽

pp. 83-93 ◽

Cited By ~ 15

Author(s):

David W. Ramming ◽

Franka Gabler ◽

Joseph L. Smilanick ◽

Dennis A. Margosan ◽

Molly Cadle-Davidson ◽

...

Keyword(s):

Powdery Mildew ◽

Resistance Genes ◽

Specific Resistance ◽

Hyphal Growth ◽

Resistance Mechanisms ◽

Hybrid Breeding ◽

Erysiphe Necator ◽

Vitis Rotundifolia ◽

Resistance Sources

Race-specific resistance against powdery mildews is well documented in small grains but, in other crops such as grapevine, controlled analysis of host–pathogen interactions on resistant plants is uncommon. In the current study, we attempted to confirm powdery mildew resistance phenotypes through vineyard, greenhouse, and in vitro inoculations for test cross-mapping populations for two resistance sources: (i) a complex hybrid breeding line, ‘Bloodworth 81-107-11', of at least Vitis rotundifolia, V. vinifera, V. berlandieri, V. rupestris, V. labrusca, and V. aestivalis background; and (ii) Vitis hybrid ‘Tamiami’ of V. aestivalis and V. vinifera origin. Statistical analysis of vineyard resistance data suggested the segregation of two and three race-specific resistance genes from the two sources, respectively. However, in each population, some resistant progeny were susceptible in greenhouse or in vitro screens, which suggested the presence of Erysiphe necator isolates virulent on progeny segregating for one or more resistance genes. Controlled inoculation of resistant and susceptible progeny with a diverse set of E. necator isolates clearly demonstrated the presence of fungal races differentially interacting with race-specific resistance genes, providing proof of race specificity in the grape powdery mildew pathosystem. Consistent with known race-specific resistance mechanisms, both resistance sources were characterized by programmed cell death of host epidermal cells under appressoria, which arrested or slowed hyphal growth; this response was also accompanied by collapse of conidia, germ tubes, appressoria, and secondary hyphae. The observation of prevalent isolates virulent on progeny with multiple race-specific resistance genes before resistance gene deployment has implications for grape breeding strategies. We suggest that grape breeders should characterize the mechanisms of resistance and pyramid multiple resistance genes with different mechanisms for improved durability.

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The Genetic Architecture of Plant Defense Trade-offs in a Common Monkeyflower

Journal of Heredity ◽

10.1093/jhered/esaa015 ◽

2020 ◽

Author(s):

Nicholas J Kooyers ◽

Abigail Donofrio ◽

Benjamin K Blackman ◽

Liza M Holeski

Keyword(s):

Growth Rate ◽

Plant Defense ◽

Genetic Linkage ◽

Genetic Architecture ◽

Life History Traits ◽

Total Concentration ◽

Defense Compounds ◽

Genetic Constraints ◽

Trade Offs ◽

Phenylpropanoid Glycosides

Abstract Determining how adaptive combinations of traits arose requires understanding the prevalence and scope of genetic constraints. Frequently observed phenotypic correlations between plant growth, defenses, and/or reproductive timing have led researchers to suggest that pleiotropy or strong genetic linkage between variants affecting independent traits is pervasive. Alternatively, these correlations could arise via independent mutations in different genes for each trait and extensive correlational selection. Here we evaluate these alternatives by conducting a quantitative trait loci (QTL) mapping experiment involving a cross between 2 populations of common monkeyflower (Mimulus guttatus) that differ in growth rate as well as total concentration and arsenal composition of plant defense compounds, phenylpropanoid glycosides (PPGs). We find no evidence that pleiotropy underlies correlations between defense and growth rate. However, there is a strong genetic correlation between levels of total PPGs and flowering time that is largely attributable to a single shared QTL. While this result suggests a role for pleiotropy/close linkage, several other QTLs also contribute to variation in total PPGs. Additionally, divergent PPG arsenals are influenced by a number of smaller-effect QTLs that each underlie variation in 1 or 2 PPGs. This result indicates that chemical defense arsenals can be finely adapted to biotic environments despite sharing a common biochemical precursor. Together, our results show correlations between defense and life-history traits are influenced by pleiotropy or genetic linkage, but genetic constraints may have limited impact on future evolutionary responses, as a substantial proportion of variation in each trait is controlled by independent loci.

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Comparative genome and transcriptome analyses of the social amoeba Acytostelium subglobosum that accomplishes multicellular development without germ-soma differentiation

BMC Genomics ◽

10.1186/s12864-015-1278-x ◽

2015 ◽

Vol 16 (1) ◽

Cited By ~ 16

Author(s):

Hideko Urushihara ◽

Hidekazu Kuwayama ◽

Kensuke Fukuhara ◽

Takehiko Itoh ◽

Hiroshi Kagoshima ◽

...

Keyword(s):

Comparative Genome ◽

Multicellular Development ◽

Social Amoeba ◽

The Social ◽

Transcriptome Analyses

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Jasmonate action in plant defense against insects

Journal of Experimental Botany ◽

10.1093/jxb/erz174 ◽

2019 ◽

Vol 70 (13) ◽

pp. 3391-3400 ◽

Cited By ~ 18

Author(s):

Jiaojiao Wang ◽

Dewei Wu ◽

Youping Wang ◽

Daoxin Xie

Keyword(s):

Transcription Factors ◽

Plant Defense ◽

Molecular Basis ◽

Recent Progress ◽

Herbivorous Insects ◽

Role Perception ◽

Rapid Synthesis ◽

Defense Systems ◽

F Box Protein ◽

Insect Attack

Abstract Herbivorous insects represent one of the major threats to sessile plants. To cope with herbivore challenges, plants have evolved sophisticated defense systems, in which the lipid-derived phytohormone jasmonate plays a crucial role. Perception of insect attack locally and systemically elicits rapid synthesis of jasmonate, which is perceived by the F-box protein COI1 to further recruit JAZ repressors for ubiquitination and degradation, thereby releasing transcription factors that subsequently activate plant defense against insect attack. Here, we review recent progress in understanding the molecular basis of jasmonate action in plant defense against insects.

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