Maryse A P Huve, Norbert Bittner, Reinhard Kunze, Monika Hilker, Mitja N P Remus-Emsermann, Luis R Paniagua Voirol, Vivien Lortzing
{"title":"Butterfly eggs prime anti-herbivore defense in an annual but not perennial Arabidopsis species.","authors":"Maryse A P Huve, Norbert Bittner, Reinhard Kunze, Monika Hilker, Mitja N P Remus-Emsermann, Luis R Paniagua Voirol, Vivien Lortzing","doi":"10.1007/s00425-024-04541-9","DOIUrl":null,"url":null,"abstract":"<p><strong>Main conclusion: </strong>Unlike Arabidopsis thaliana, defenses of Arabidopsis lyrata against Pieris brassicae larval feeding are not primable by P. brassicae eggs. Thus, egg primability of plant anti-herbivore defenses is not phylogenetically conserved in the genus Arabidopsis. While plant anti-herbivore defenses of the annual species Arabidopsis thaliana were shown to be primable by Pieris brassicae eggs, the primability of the phylogenetically closely related perennial Arabidopsis lyrata has not yet been investigated. Previous studies revealed that closely related wild Brassicaceae plant species, the annual Brassica nigra and the perennial B. oleracea, exhibit an egg-primable defense trait, even though they have different life spans. Here, we tested whether P. brassicae eggs prime anti-herbivore defenses of the perennial A. lyrata. We exposed A. lyrata to P. brassicae eggs and larval feeding and assessed their primability by (i) determining the biomass of P. brassicae larvae after feeding on plants with and without prior P. brassicae egg deposition and (ii) investigating the plant transcriptomic response after egg deposition and/or larval feeding. For comparison, these studies were also conducted with A. thaliana. Consistent with previous findings, A. thaliana's response to prior P. brassicae egg deposition negatively affected conspecific larvae feeding upon A. thaliana. However, this was not observed in A. lyrata. Arabidopsis thaliana responded to P. brassicae eggs with strong transcriptional reprogramming, whereas A. lyrata responses to eggs were negligible. In response to larval feeding, A. lyrata exhibited a greater transcriptome change compared to A. thaliana. Among the strongly feeding-induced A. lyrata genes were those that are egg-primed in feeding-induced A. thaliana, i.e., CAX3, PR1, PR5, and PDF1.4. These results suggest that A. lyrata has evolved a robust feeding response that is independent from prior egg exposure.</p>","PeriodicalId":20177,"journal":{"name":"Planta","volume":null,"pages":null},"PeriodicalIF":3.6000,"publicationDate":"2024-10-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11450040/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Planta","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1007/s00425-024-04541-9","RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"PLANT SCIENCES","Score":null,"Total":0}
引用次数: 0
Abstract
Main conclusion: Unlike Arabidopsis thaliana, defenses of Arabidopsis lyrata against Pieris brassicae larval feeding are not primable by P. brassicae eggs. Thus, egg primability of plant anti-herbivore defenses is not phylogenetically conserved in the genus Arabidopsis. While plant anti-herbivore defenses of the annual species Arabidopsis thaliana were shown to be primable by Pieris brassicae eggs, the primability of the phylogenetically closely related perennial Arabidopsis lyrata has not yet been investigated. Previous studies revealed that closely related wild Brassicaceae plant species, the annual Brassica nigra and the perennial B. oleracea, exhibit an egg-primable defense trait, even though they have different life spans. Here, we tested whether P. brassicae eggs prime anti-herbivore defenses of the perennial A. lyrata. We exposed A. lyrata to P. brassicae eggs and larval feeding and assessed their primability by (i) determining the biomass of P. brassicae larvae after feeding on plants with and without prior P. brassicae egg deposition and (ii) investigating the plant transcriptomic response after egg deposition and/or larval feeding. For comparison, these studies were also conducted with A. thaliana. Consistent with previous findings, A. thaliana's response to prior P. brassicae egg deposition negatively affected conspecific larvae feeding upon A. thaliana. However, this was not observed in A. lyrata. Arabidopsis thaliana responded to P. brassicae eggs with strong transcriptional reprogramming, whereas A. lyrata responses to eggs were negligible. In response to larval feeding, A. lyrata exhibited a greater transcriptome change compared to A. thaliana. Among the strongly feeding-induced A. lyrata genes were those that are egg-primed in feeding-induced A. thaliana, i.e., CAX3, PR1, PR5, and PDF1.4. These results suggest that A. lyrata has evolved a robust feeding response that is independent from prior egg exposure.
主要结论:与拟南芥不同,拟南芥对黄刺茧蜂幼虫取食的防御能力不能被黄刺茧蜂卵激发。因此,在拟南芥属中,植物抗食草动物防御系统的卵启动性在系统发育上并不保守。虽然研究表明一年生拟南芥的植物抗食草动物防御系统可被拟南芥刺尾蝇卵引诱,但尚未对系统发育上密切相关的多年生拟南芥的引诱性进行研究。以前的研究表明,与拟南芥密切相关的野生十字花科植物物种--一年生黑芸薹属和多年生拟南芥--表现出卵可引诱的防御特性,尽管它们的寿命不同。在这里,我们测试了 P. brassicae 的卵是否能激发多年生 A. lyrata 的抗食草动物防御能力。我们将 A. lyrata暴露于黄刺椿虫卵和幼虫的喂食中,并通过(i)确定在有黄刺椿虫卵沉积和无黄刺椿虫卵沉积的植物上取食后黄刺椿幼虫的生物量,以及(ii)调查植物在虫卵沉积和/或幼虫取食后的转录组反应,来评估它们的首要性。为了进行比较,这些研究也是以大连农杆菌(A. thaliana)为对象进行的。与之前的研究结果一致,连翘对之前铜绿微囊藻卵沉积的反应会对同种幼虫取食连翘产生负面影响。然而,在拟南芥中没有观察到这种情况。拟南芥对 P. brassicae 卵的反应是强烈的转录重编程,而 A. lyrata 对卵的反应可以忽略不计。与拟南芥相比,拟南芥对幼虫摄食的反应表现出更大的转录组变化。在强烈的进食诱导 A. lyrata 基因中,有那些在进食诱导的 A. thaliana 中被卵诱导的基因,即 CAX3、PR1、PR5 和 PDF1.4。这些结果表明,A. lyrata 已经进化出一种独立于先前卵暴露的强大摄食反应。
期刊介绍:
Planta publishes timely and substantial articles on all aspects of plant biology.
We welcome original research papers on any plant species. Areas of interest include biochemistry, bioenergy, biotechnology, cell biology, development, ecological and environmental physiology, growth, metabolism, morphogenesis, molecular biology, new methods, physiology, plant-microbe interactions, structural biology, and systems biology.