Philippa Kaur

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Genome skimming provides robust phylogenyPioneering molecular phylogenetic studies in Sepiolida that used short regions of a few mitochondrial and nuclear genes failed to resolve the relationship of major clades9,22,23. To increase the number of phylogenetically informative sites, Sanchez et al.11 sequenced and analyzed the transcriptomes of multiple species of Euprymna Steenstrup, 1887, related bobtail squids including Sepiola parva Sasaki, 1913 and Sepiola birostrata Sasaki, 1918, and several bottletail squids. They found that S. parva grouped with the Euprymna species to the exclusion of S. birostrata, and further morphological analysis led to the formal redefinition of the genus Euprymna and the reassignment of S. parva Sasaki, 1913 to Euprymna parva11. The following year, in an exhaustive study of hectocotylus structure, Bello19 proposed that Euprymna be split back into the original Euprymna Steenstrup, 1998 and a newly defined genus, Eumandya Bello 2020 that contains E. parva Sasaki, 1913 and E. pardalota Reid 2011, two taxa whose arms have two rows of suckers rather than four as in other Euprymna species. Similarly, Bello introduced a new genus, Lusepiola Bello, 2020 that has the effect of renaming Sepiola birostrata Sasaki, 1918 as Lusepiola birostrata. For clarity, we adopt the finer-grained nomenclature of Bello below, but happily note that E. parva and E. pardalota have the same abbreviations in both the notation of Sanchez et al.11 and Bello19.Sanchez et al.11 also emphasized the need for more taxon sampling, careful species assignment, and the inclusion of more informative sites when studying this group of cephalopods. However, the distribution and lifestyle of many lineages of Sepiolida makes the collection of fresh tissue for RNA sequencing very challenging. To overcome this limitation, we sequenced the genomic DNA of several Sepiolida species at shallow coverage up to 3.6× and accessed by this way several mitochondrial and nuclear loci. Most of our samples were carefully identified at the species level based on morphological characters.We recovered the mitochondrial genomes of the species targeted in this study and annotated the 13 protein-coding genes, 22 tRNAs, and two rRNAs (although only the conserved region of the large and small rRNA was obtained for Rondeletiola minor Naef, 1912).Additionally, we also downloaded the complete mitochondrial genomes of S. austrinum and Idiosepius sp., and the transcriptome of E. tasmanica available in the NCBI database. The transcriptome of E. tasmanica was used to extract its complete set of mitochondrial protein-coding genes. We could reconstruct the mitochondrial gene order for all species with complete mtDNA genomes, but we observed no re-arrangement for members of Sepiolidae, and only Sepiadarium austrinum deviated from the arrangement seen in all other Sepiadariidae (Fig. S1).To complement the mitochondrial-based evolutionary history, we also annotated several nuclear loci. As ribosomal gene clusters are present in numerous copies, they were successfully retrieved for almost all the species, except for 28S of the Sepiadariidae sp. specimen, which appeared problematic and was excluded.By mapping reads to the reference genome of E. scolopes, we obtained 3,279,410 loci shared between at least two species and further selected 5215 loci presented in most of our Sepiolidae species, but allowed some missing data in the Euprymna + Eumandya clade. This was done because the phylogenetic relationships of the Euprymna + Eumandya species were previously described in detail in Sanchez et al.11 using transcriptome data. Out of the 5215 loci, 5164 loci had a per-site coverage ranging between two and five. After trimming and removal of regions without informative sites, 577 loci remained. These ultraconserved loci had lengths ranging between 10 and 690 base pairs (bp), with an average of 65 bp. Our alignment matrix had a length of 37,512 bp and consisted of 16,495 distinct site patterns, and variable sites between 1 and 130 bp with an average value of 7 bp. We expected a low value of variable sites because these regions are highly conserved.We considered resolved nodes to be those with the ultrafast bootstrap support and posterior probability larger than 95% and 0.9, respectively. Only the very unresolved nodes were found based on the mito_nc matrix (Fig. 1). However, among the species in these nodes, Adinaefiola ligulata Naef, 1912 was well supported with amino acid sequences from mitochondrial genes (posterior probability of 1 and 94% bootstrap support) and partially by the ultraconserved loci (posterior probability of 1, but only 85% bootstrap support) as sister to the Sepiola clade (Figs. 2 and S2). Moreover, compared to the mito_nc matrix and with identical topology, mito_aa and UCEbob fully resolved the relationship of the Indo-Pacific and Mediterranean Sea Sepiolinae. The tree generated by the nuclear_rRNA produces a topology with most nodes unsupported (Fig. S3), suggesting these markers are too conserved for assessing the relationships among this group.Fig. 1: Phylogeny of Sepiolida based on nucleotide sequences from the mitochondria (mt_nc matrix).The topology of the maximum likelihood tree is shown. Numbers by the nodes indicate bootstrap support and the Bayesian posterior probabilities. Values of bootstrap support and posterior probabilities above 95% and 0.95, respectively, are not shown. (*) indicates that the node was resolved with the mito_aa and UCEbob matrices. (+) indicate that A. ligulata is sister to Sepiola using mito_aa with ultrafast bootstrap support of 94% and a posterior probability of 1. Abbreviations: IP, Indo-Pacific Ocean; MA, Mediterranean Sea, and the Atlantic Ocean.Full size imageFig. 2: Phylogenetic tree of Sepiolida based on conserved nuclear loci (UCEbob matrix).The topology of the maximum likelihood tree is shown. Numbers in by the nodes indicate the bootstrap support and the Bayesian posterior probability. Values of bootstrap support and posterior probabilities above 95% and 0.95, respectively, are not shown. IP, Indo-Pacific Ocean; MA, Mediterranean Sea, and the Atlantic Ocean.Full size imageUsing the UCEbob matrix, the topology and supported relationships of Euprymna + Eumandya species resemble those reported in Sanchez et al.11 using transcriptome sequences, proving our protocol valid when using low coverage sequencing and when a reference genome of the closest related species is available.The position of R. minor showed discordance between mitochondrial and nuclear datasets. Using the mitochondrial matrices, R. minor rendered the Sepietta Naef, 1912 clade paraphyletic, whereas using the UCEbob and rRNA_nc matrices, R. minor appeared sister to the Sepietta clade. These relationships were resolved in both mitochondrial and nuclear-based trees and require further investigation with more DNA markers and a wider population sampling.Molecular systematics of Sepiolida cladesUsing the complete mitochondrial genome, ribosomal nuclear genes, and ultraconserved loci, we recovered the monophyly of the two families of the order Sepiolida—Sepiadariidae and Sepiolidae9,24—and the monophyly of the three described subfamilies of the family Sepiolinae. However, contrary to what is proposed based on morphology in Young24, the Rossinae is not sister to all the remaining Sepiolidae but rather is sister to Heteroteuthinae, although this is unresolved in the UCE phylogeny. With the lack of systematic work on these subfamilies, our robust phylogenetic backbone in Sepiolida using new samples carefully identified by morphology and with museum vouchers, represents a notable advance to clarify the evolution of morphological traits in major clades within the family.Based on morphological characters of the hectocotylus, Bello19 recently split the polyphyletic Sepiola Leach 1817 into Lusepiola, Adinaefiola, and Boletzkyola, reserving Sepiola for the S. atlantica group sensu Naef 1923. These newly defined clades are consistent with our molecular phylogeny here and in Sanchez11, who also noted the polyphyly of Sepiola in the Indo-Pacific lineage.We find that Sepiolinae can be robustly split into two geographically distinct tribes: one that comprises species with known distribution in the Indo-Pacific region (tribe Euprymmini new tribe, defined as Sepiolinae with a closed bursa copulatrix, type genus Euprymna) and the other including all the Mediterranean and Atlantic species (tribe Sepiolini Appellof, 1989, defined here as Sepiolinae with an open bursa copulatrix, type genus Sepiola). Our molecular relationship is consistent with 13 of the 15 apomorphies used in the cladogram shown in Fig. 21 in Bello19. The other two proposed apomorphies in Bello (his apomorphic characters 4 and 6) group two IP lineages, Lusepiola and Inioteuthis, in a clade with species from the Mediterranean and Atlantic. Such relationships contradict our Euprymmini-Sepiolini sister relationship. Moreover, according to our phylogeny, apomorphy 6 of Bello, characterized by the participation of ventral and dorsal pedicels in the formation of the hectocotylus copulatory apparatus, implies that the male ancestor of Sepiolinae had a more developed hectocotylus that was simplified in the Euprymna and Eumandya clades.Among euprymins, we confirmed the monophyly of Euprymna Steenstrup 1887 as found previously by transcriptome analysis11. We also support the monophyly of Eumandya Bello, 2020 (Figs. 1 and 2), grouping the type species E. pardalota with E. parva along with the unnamed “Type 1” Ryukyuan species of Sanchez et al.11, for which only hatchlings were available. The phylogenomic grouping of Ryukyuan “Type 1” with Eumandya suggests that when its adults are found (or hatchlings are raised to maturity), its arms will carry two rows of suckers. We also found an adult of a Ryukyuan “Type 4” (extending the notation of Sanchez et al.11 in the coastal waters of Kume Island, that groups with E. scolopes from Hawaii, suggesting a divergence based on geographic isolation in the North Pacific. We also find that Lusepiola birostrata (formerly Sepiola birostrata) is grouped with Inioteuthis japonica as sister to a clade containing Euprymna, Eumandya, and an unnamed sepioline from Port Kembla, at the northeast of Martin Island in Australian waters.Among the sepiolins, we confirm the monophyly of Sepietta (only for nuclear-genome-based trees, see below). Adinaefiola, another genus erected by Bello19, with Sepiola ligulata Naef 1912 as its type species; was found sister to the Sepiola clade, but only in the tree based on amino acid mitochondrial sequences (mito_aa matrix) with a bootstrap value of 94% and a posterior probability of 1 (Fig. S2).Outside the sepiolines, members of the subfamily Heteroteuthinae are the most elusive and underrepresented in studies of cephalopod systematics due to their oceanic lifestyles. The placement of several heteroteuthin remains controversial. Lindgren et al.9, with six nuclear and four mitochondrial genes downloaded from GenBank found that Sepiolina Naef, 1912 was sister to Heteroteuthis Gray, 1849 + Rossia Owen, 1834+ Stoloteuthis Verril, 1881; rendering the subfamily Heteroteuthinae polyphyletic. In contrast, our work supports the monophyly of Heteroteuthinae by including Stoloteuthis and Heteroteuthis in this subfamily, while Rossia was placed within the Rossinae (Figs. 1, 2, S2). Members of Heteroteuthinae included in this study formed a sister group to a monophyletic Rossinae (Figs. 1, 2, S2). Semirossia, however, rendered the Rossia clade paraphyletic. Further discussion about the position of Semirossia is difficult because of the lack of information about the original source of this specimen in Kawashima et al.25.The light organ and luminescence evolutionBobtail squids are thought to use the bioluminescence of their light organ to camouflage them from predators while foraging and swimming at night through a mechanism called counter-illumination. This has been researched extensively using E. scolopes as a model system26,27,28. Unfortunately, the limited number of sequences available and the misidentification of bobtail squids in the GenBank database11,29,30 have hindered our understanding of the light organ evolution in the whole taxon.Our robust phylogeny and Bayesian reconstruction of ancestral bioluminescence clarify how the light organ and its luminescence have evolved in the family Sepiolidae. Members of Sepiolinae comprise neritic and benthic adults with bilobed light organs, except for two genera: Inioteuthis from the Indo-Pacific region, and the Sepietta species from the Mediterranean Sea and the Atlantic waters. The ancestor of the Sepiolinae very likely possessed a bilobed light organ that harbored luminescent symbiotic bacteria (Fig. 3). This character persisted until the ancestor of the euprymnins and sepiolins. Assuming that R. minor is sister to the Sepietta clade (as shown with the nuclear-based dataset, Fig. 2), it is clear that the bilobed light organ was lost once in Inioteuthis and Sepietta, and simplified to a rounded organ in R. minor. The alternative scenario, where R. minor renders the Sepietta clade paraphyletic (based on mitochondrial matrices, Fig. 1), is less plausible as it implies that the light organ was lost twice in the Sepietta group, once in S. obscura and then in the ancestor of S. neglecta and S. oweniana; or alternatively that it was lost in the ancestor of Sepietta-Rondelentiola followed by a reversion of this character in the lineage of Rondelentiola.Fig. 3: Ancestral character reconstruction (ASR).ASR of (a) the shape of the light organ and (b) the origin of luminescence in the Sepiolida. The posterior probability of each state is shown as a pie chart, mapped tree generated in BEAST (based on mito_nt matrix, see below), with the outgroups removed.Full size imageThe light organ is also present in all members of Heteroteuthinae. These bobtails are pelagic as adults, and their light organ appears as a single visceral organ rather than the bilobed form found in nektobenthic Sepiolinae. In contrast to the bacteriogenic luminescence of the light organ in E. scolopes31, previous studies in H. dispar3 failed to detect symbiotic bacteria and suggested that the luminescence has an autogenic origin. Thus, it seems plausible that the monophyly of Heteroteuthinae found in our study supports the findings in Lindgren et al.9 for convergent evolution of autogenic light organs associated with pelagic lifestyle in many squid, octopus, and Vampyroteuthis Chun, 19039,32.Divergence time of SepiolidaThe absence of fossils for this group limited our calculations of divergence time to the use of secondary calibrations. These calibrations can provide more accurate estimates depending on the type of primary calibrations that are used33. We retrieved secondary calibrations from previous estimations in Tanner et al.15, who used eleven fossil records spanning from coleoids to gastropods in transcriptome-based phylogenetic trees. Specifically, we used the time for the splits of Sepia esculenta and S. officinalis (~91 Mya), Idiosepiidae, and Sepiolida (~132 Mya) and the origin of the Decapodiformes (root age, ~174 Mya) (Fig. 4). These calibrations and our robust phylogenetic trees allow us to investigate the events that shape the divergence of some clades of the order Sepiolida (Figs. 4,  S4).Fig. 4: A chronogram of sepiolids using complete mitochondrial genes.Red dots indicate the nodes with secondary calibrations. K-Pg, refers to the Cretaceous-Paleogene boundary and MSC, to the Messinian salinity crisis.Full size imageSepiolida appeared before the Cretaceous-Paleogene extinction event34, during the middle Mesozoic around 94 Mya (95% HPD = 60.61–130.72). This time frame coincides with the rapid diversification of several oegopsida lineages15,35. Our molecular estimates also indicate that radiation of Sepiolidae and Sepidariidae occurred around the Cretaceous-Paleogene boundaries and is concurrent with the rapid diversification of modern marine percomorph fishes around the globe, after the extinction of Mesozoic fishes36,37.Among the species of Sepiolinae collected in the Mediterranean Sea for this study, only Sepiola robusta Naef, 1912, and Sepiola affinis Naef, 1912 are endemic to the Mediterranean Sea38. The distribution of the other species includes the Mediterranean Sea, North Atlantic Ocean, East Atlantic Ocean, and/or up to the Gulf of Cadiz. The confidence intervals for the split between the Mediterranean-Atlantic and Indo-Pacific lineages, and their diversification, overlap during the early Eocene to the beginning of the Oligocene (Figs. 4 and  S4). This time interval coincides with the end of the Tethys Sea, which separated the Indo-Pacific from the Mediterranean and Atlantic region through the Indian-Mediterranean Seaway39,40. This separation also influenced the divergence of loliginid clades, coinciding with the split between the Eastern Atlantic plus Mediterranean clade (Loligo, Afrololigo, Alloteuthis) and Indo-Pacific clade (Uroteuthis and Loliolus) (~55 Mya based on Fig. 2 in Anderson and Marian41).Our chronogram indicates that the ancestor of Sepiolinae arose prior to the early Eocene around 46 Mya (95% HPD = 25.16–69.49) (Fig. 4), already possessing a bilobed light organ hosting luminescent bacteria (Fig. 3). We estimate that the split between S. affinis and S. intermedia occurred around 2.62 Mya (95% HPD = 0.3–7.4) (Fig. 4) during the end of the Zanclean period, when the Atlantic Ocean refilled the Mediterranean after the Messinian salinity crisis42,43. While S. affinis is a coastal species with a narrow depth limit, S. intermedia inhabits a wider range of deeper waters. It is possible that two populations of their ancestor, each adapted to a different ecological niche and diverged sympatrically in Mediterranean waters, and, after the speciation, S. intermedia extended its distribution outside the Mediterranean to the Gulf of Cadiz44.We also estimate that the split between H. dispar Rüppell, 1844 and H. hawaiiensis (Berry, 1909) occurred around 2.4 Mya (95% HPD = 0.46–5.88), coinciding with the closure of the Isthmus of Panama around 2.8 Mya45. Surveys of these species found H. hawaiiensis in the North Pacific and H. dispar in the North Atlantic Ocean and Mediterranean Sea46. A recent speciation event might be the reason for the lack of morphological differences between the two species46. Thus, these species may be rendered as cryptic species, a phenomenon increasingly reported in oceanic cephalopods47. The sister species of this cryptic species complex, H. dagamensis Robson, 1924, appeared before, around 6 Mya, and is reported with broad distribution in the South Atlantic Ocean off South Africa, the Gulf of Mexico, North Atlantic Ocean between Ireland and Newfoundland in Canada, and the South Pacific Ocean off New Zealand48,49,50.The origin of the Heteroteuthis ancestor of H. dispar, H. hawaiiensis, and H. dagamensis can be placed in the Pacific Ocean. After the formation of the Isthmus of Panama, the northern population of Heteroteuthis might have split into H. hawaiiensis in North Pacific and H. dispar in the Atlantic Ocean (from where it also migrated to the Mediterranean Sea). Meanwhile, the formation of the equatorial currents isolated the southern population of Heteroteuthis and gave rise to H. dagamensis. Then, H. dagamensis extended its distribution from the Southern Pacific to the South Atlantic Ocean, the North Atlantic waters, and the Gulf of Mexico. Analysis of molecular species delimitation, however, suggests that H. dagamensis includes cryptic lineages among Atlantic and New Zealand populations30.While the origin of Heteroteuthis might also be in the Atlantic Ocean, the higher diversity of heteroteuthins in the Pacific (H. hawaiiensis, H. dagamensis, H. ryukyuensis Kubodera, Okutani and Kosuge, 2009, H. nordopacifica Kubodera and Okutani, 2011, and an unknown H. sp. KER (only known from molecular studies49)) than at the Atlantic (H. dispar and H. dagamensis), make its origin at the Atlantic less plausible. Moreover, the Atlantic Heteroteuthis were found nested within Heteroteuthinae species from the Pacific, supporting Pacific Ocean origin (Figs. 1, 4).By sequencing the genomic DNA of sepiolids at low coverage, we recovered complete mitochondrial genomes and nuclear ribosomal genes for most of our collections. Furthermore, mapping reads to the reference genome of E. scolopes allowed us to retrieve additional nuclear-ultraconserved regions. We demonstrate that these nuclear and mitochondrial loci are useful to reconstruct robust phylogenetic trees, especially when the transcriptomes of specimens are difficult to collect, as for sepiolids inhabiting oceanic environments. Finally, our study integrated genomic DNA sequencing with confident morphological identification, which helped to reconstruct the ancestral character of the light organ and its luminescence in sepiolids, and clarify how major lineages have evolved, establishing the existence of distinct Indo-Pacific and Mediterranean-Atlantic subfamilies of Sepiolinae. Our collections and genomically anchored phylogenies will provide a reliable foundation classification of sepiolids for future studies. More

To determine whether exposure to (Z)-11-16:Ald induced detectable defence-related responses in B. nigra, we investigated the amount of feeding damage to plants and the volatile emissions of plants exposed to volatilised pure compound. Contrary to our hypothesis, P. xylostella larvae fed more on plants previously exposed to (Z)-11-16:Ald at biologically relevant levels than on controls, suggesting that exposure to (Z)-11-16:Ald might increase the susceptibility of plants to future herbivory. Earlier work investigating the responses of plants to insect sex pheromone showed that exposure primed defences14,16, resulting in higher volatile emissions13, and lower feeding12. Our results are different to these findings and suggest alternative ecological effects of detecting insect pheromone to those reported earlier.The greater feeding on (Z)-11-16:Ald-exposed plants compared to controls could relate to the differences in volatile emissions of the differently treated plants. Although there were no detectable differences in volatile emissions between exposed plants and controls immediately after (Z)-11-16:Ald-exposure, there were differences after a subsequent 24 h of feeding. The difference could be due to (Z)-11-16:Ald-induced changes in the plant directly affecting herbivore-induced volatile emission, or could be related to altered plant nutrition or defences leading to an increase in the leaf area consumed by herbivores and a consequent difference in induction of volatile emissions. Thus (Z)-11-16:Ald could potentially alter plant defences and in doing so increase the survival of eggs and future hatched larvae. It has earlier been shown in Arabidopsis thaliana that application of Pieris brassicae or Spodoptera littoralis egg extract onto leaves reduced the induction of genes related to defence against insects after caterpillar feeding23. However, at this stage our data does not allow us to further explore these ecological hypotheses. Additional studies would need to test in greater detail the deposition of eggs, the hatching of eggs, and performance and survival of developing larvae of plants exposed to (Z)-11-16:Ald.The observation of changes in feeding amount and plant volatile responses prompted us to examine the early and late signaling events in response to (Z)-11-16:Ald exposure. The results showed that exposure to (Z)-11-16:Ald induced a transmembrane depolarisation by plants. The depolarisation of the plasma membrane potential is known to be the first detectable event in the detection of a biotic or abiotic stress19. We estimated the detection threshold of the pheromone to be a concentration between 25 and 10 ppm. A lower level of transmembrane depolarisation was observed when plants were exposed to (Z)-11-16:Ac, hence (Z)-11-16:Ald appears to be the most phytoactive component of the P. xylostella sex pheromone. However, it remains unclear how specific the plant response is to the (Z)-11-16:Ald, which should be further elucidated by comparison with aldehydes that have a more similar chemical structures.The plasma membrane is the only cellular structure in direct contact with the environment, which makes it critical for sensing environmental stimuli and initiating a cascade of events that eventually leads to a specific response21. As demonstrated in Arabidopsis, Vm depolarisation depends on a cascade of events that include changes in [Ca2+]cyt and the production of ROS24. We found that 50 ppm and 100 ppm of (Z)-11-16:Ald increased both the [Ca2+]cyt and the production of ROS. Moreover, we demonstrated that the increased ROS detected by CLSM were associated with the increased expression of reactive oxygen species (ROS)-mediated genes and ROS-scavenging enzyme activity. ROS participate in cell oxidation, during which H2O2 is produced and later regulated by ROS-scavenging enzymes involved in its degradation to protect cells from oxidative stress25,26. The production of H2O2 is potentially harmful and can result in oxidation in the cells of aerobic living organisms27. It is also an important component of the signalling network in plants28,29 and takes part in plant defence in response to environmental stress30,31. Several plant species trigger localized cell death by producing ROS at oviposition sites on leaves, which has been shown to be associated with an increase in egg mortality or a reduction of larval survival rate32. Recently, Bittner and colleagues demonstrated that when plants are previously exposed to the female pine sawfly (D. pini) sex pheromone, they produce H2O2 and induce defence-related genes faster after egg deposition on leaves, compared to plants that have not been exposed to the pheromone15. They suggested that the sex pheromone acted as an environmental cue indicating to plants that there would be future egg deposition on needles and subsequent herbivory. Plants then responded to it by producing H2O2, which formed necrotic tissue and reduced survival of eggs. Taken together with our observations, it is possible that the (Z)-11-16:Ald also primes B. nigra plant defences by producing H2O2 as a defensive mechanism to limit future egg deposition. It was shown that B. nigra plants induce the necrosis of cells located at the oviposition site of Pieris rapae and Pieris napi33, which can support this hypothesis. Contrary to the hypothesis of defence induction, B. nigra plants exposed to (Z)-11-16:Ald received more herbivore-feeding damage than control plants, but further investigations are needed to determine whether the production of H2O2 following exposure to (Z)-11-16:Ald would reduce subsequent egg deposition or hatching.Interestingly, early signalling events following the exposure to (Z)-11-16:Ald are analogous to the responses induced by biotic stress such as herbivore-wounding20,22, and in response to HIPVs21. For example, exposure to HIPVs resulted in a depolarisation of the plasma membrane (Vm)34,35 due to the entrance of calcium (Ca2+) into the cytosol of cells34. The detection of HIPVs results in transcriptional36,37, metabolic and physiological changes in plants38. Several studies have shown that plants perceiving HIPVs deploy faster and stronger chemical defences upon subsequent stress8,9, which can negatively affect herbivorous insects39. The observed action of (Z)-11-16:Ald is typical to that of insect and mite elicitors21,40,41. However, it is notable that to determine if (Z)-11-16:Ald induced detectable responses in B. nigra plants, whole plants were exposed to vapourised (Z)-11-16:Ald for 24 h, while to determine early and late signalling events following exposure to (Z)-11-16:Ald we applied 100 ppm in aqueous state for 30 min to 1 h (Table S2). While we used a biologically realistic scenario with a realistic concentration of pheromone for the whole plant responses the in vitro experiments focussed on mechanisms do not represent biologically accurate scenarios and utilised high concentrations of pheromone. Future studies should bridge this methodological gap by utilising more biologically realistic scenarios in mechanism elucidation.(Z)-11-16:Ald has been found to be a main constituent of pheromones in many moth species from the Noctuidae family including the corn earworm Helicoverpa zea42, which is the second-most important economic pest species in North America43. Many plants that have co-evolved with the Noctuidae could have the ability to detect (Z)-11-16:Ald. Prior to this study, the ability of plants to detect insect-emitted volatiles had been reported for two species: a perennial plant, S. altissima, and a tree, P. sylvestris. We can now tentatively add an annual plant, B. nigra, to the list. These studies suggest that the ability to detect insect-emitted volatiles has widely evolved in a large variety of plant families, and highlight the need to determine how widespread this trait is. Further studies should also determine the threshold and distance of detection and the ecological consequences of this detection.In summary our results indicate for the first time that exposing B. nigra plants to volatile (Z)-11-16:Ald increases the susceptibility of plants to feeding by P. xylostella larvae and induces an alteration in herbivore-induced volatile emissions. Further mechanistic experiments conducted in vitro using high doses of pheromone indicated that exposure to (Z)-11-16:Ald induces responses in receiver plants that are characterised by a depolarisation of Vm, an increase in [Ca2+]cyt and production of H2O2 leading to an increase in ROS-mediated gene expression and ROS scavenging-enzyme activity, which are typical responses to insect elicitors. This study supports recent findings showing that plants can detect insect-emitted volatiles. However, further research should be conducted to determine an accurate dose response of whole plants to volatile pheromone and the specificity of the response to this particular aldehyde.Materials and methodsThe study complied with local and national regulations.PlantsBrassica nigra (black mustard) seeds were collected from wild populations in the Netherlands (supplied by E. Poelman, Wageningen University). For experiment 1, conducted in Kuopio (Finland), plants were grown in plastic pots (8 × 8 cm) containing a mix of peat, soil and sand (3:1:1), in plant growth chambers (Weiss Bio 1300 m, Germany) with a 16L: 8D and light intensity of 250 µmol m−2 s−1. The temperature was maintained at 21 °C with 60% relative humidity during the day and decreased to 16 °C with 80% RH during the night time. Plants were watered every day and fertilized twice per week with a 0.1% solution containing nitrogen, phosphorous and potassium in a 19:4:20 ratio (Kekkilä Oyj, Finland).For experiments conducted in Turin (Italy) (Experiments 2 to 4), plants were grown in plastic pots (8 × 8 cm) containing a mix of peat, soil (Klasmann-Deilmann, Germany), sand (Vimark, Italy) and vermiculite (Unistara, Italy), in a climate-controlled room at 22 ± 1 °C, 16L:8D with light intensity of 250 µmol m−2 s−1. Three and four-week-old plants were used for all the experiments.Insects and synthetic compoundsPlutella xylostella were reared on broccoli (B. oleracea var. italica) with an artificial light–dark cycle of 16L:8D at 22 ± 0.5 °C.Synthetic (Z)-11-hexadecenal [(Z)-11-16:Ald] and (Z)-11-hexadecenyl acetate [(Z)-11-16:Ac] (isomeric purity 93%), were purchased from Pherobank (Wageningen, The Netherlands).Exposure of plants to treatmentsA 100 ppm solution of synthetic (Z)-11-16:Ald diluted in dichloromethane was prepared and 100 µl of the solution was injected into a rubber septum (7 mm O.D; Sigma-Aldrich) and left for 30 min for the dichloromethane to evaporate. As a solvent control, 100 µl of dichloromethane was deposited on a rubber septum, and left to evaporate for 30 min. A second control, without the rubber septum and dichloromethane, was also set up. Either treatment or control septa were enclosed in 0.5 L glass jars connected with Teflon tubing to plastic bags (Polyethylene terephthalate; overall dimensions 28 × 35 cm; Look Isopussi Eskimo oy, Finland). Plants were enclosed in the PET bags, that were previously baked for 1 h at 120 °C. For 24 h, a clean air flow was passed into the treatment or control glass jars and then into the bags containing the plants (Fig. S1 and Table S2).Volatile collections and feeding assaysAfter 24 h of exposure to the treatments, jars containing the rubber septa were disconnected from the plants, and a first VOC sampling was made before adding 22 first and second instar P. xylostella larvae were added to each plant for 24 h. After 24 h of feeding, volatile compounds were collected by dynamic headspace sampling (Fig. S1). VOCs were trapped by pulling clean air at 0.22 L min−1 for one hour through steel tubes filled with 200 mg Tenax TA 60/80 adsorbent (Markes International Ltd, UK) using a vacuum pump (KNF, Germany). The collected volatiles were thermally desorbed and analysed by gas chromatography-mass spectrometry (Agilent 7890A GC, and Agilent MS model 5975C VL MSD; New York, USA). Trapped compounds were desorbed with a thermal desorption unit (TD-100; Markes International Ltd, Llantrisant, UK) at 250 °C for 10 min, and cryofocused at − 10 °C in splitless mode onto an HP‐5 capillary column (50 m, 0.2 mm i.d, 0.5 μm film thickness; Hewlett‐Packard). The oven temperature programme was held at 40 °C for 1 min and then ramped 5 °C min−1 to 210 °C, and then further ramped at 20 °C min−1 to 290 °C. The carrier gas was helium, the transfer line temperature to the MSD was 300 °C, the ionization energy was 70 eV, and the full scan range was 29–355 m/z. We identified volatiles by comparison with a series of analytical standards (Sigma-Aldrich, Germany) and by comparison of their mass spectra to those in the NIST and Wiley 275 mass spectral libraries. Compound quantification was based on Total Ion Chromatograms (TIC) and according to the responses of analytical standards. Emission rates (ER) were calculated with the formula ER = X*Ai/Dw*t*Ao. ER was expressed in ng gDW−1 h−1, X was the compound quantity (ng), Ai and Ao were the inlet and outlet air flows (mL min-1), respectively, t was the sampling time of one hour and Dw is the dry weight of the plant sampled (g).After the volatile collection, we placed leaves of plants on A4 paper for scaling and digitally photographed them. Plants were then dried in paper bags in an oven at 60 °C for 3 days. The leaf area consumed by larvae was calculated using the LeafAreaAnalyzer software (https://github.com/EmilStalvinge/LeafAreaAnalyser; emilstalvinge@gmail.com).Transmembrane potential (Vm) measurementsLeaf segments (0.5 cm2) of three individual B. nigra plants were placed in Eppendorf tubes for 1 h with either 1 ml of (Z)-11-16:Ald solution, (Z)-11-16:Ac solution or control (Table S2). Vm was determined by inserting an electrode into a plant leaf segment following a method detailed earlier44. Vm variations were measured upon perfusion of four concentrations: 10, 25, 50, and 100 ppm diluted in MES buffer (pH 6.5) + 0.1% Tween 20 (V/V). A solution of MES buffer (pH 6.5) + 0.1% Tween 20 (V/V) was used as control. Vm values were recorded every five seconds.Determination of intracellular calcium variations using confocal laser scanning microscopy (CLSM) and Calcium OrangeCalcium Orange dye (stock solution in DMSO, Molecular Probes, Leiden, The Netherlands) was diluted in 5 mM MES-Na buffer (pH 6.0) to a final concentration of 5 µM. This solution was applied to B. nigra leaves attached to the plant as previously reported20,24,45. After 1 h incubation with Calcium Orange, the leaf was mounted on a Leica TCS SP2 (Leica Microsystems Srl, Milan, Italy) multiband confocal laser scanning microscope (CLSM) stage, without separating the leaf from the plant, in order to assess the basic fluorescence levels as control. A 50 µl application of either 50 or 100 ppm (Z)-11-16:Ald was made and after 30 min the calcium signature was observed. The microscope operates with a Krypton/Argon laser at 543 nm and 568 nm wavelengths: the first wavelength excites Calcium Orange, resulting in green fluorescence and the second mainly excites chlorophyll, resulting in red fluorescence. All images were obtained with an objective HCX APO 40 × immersed in water with a numeric aperture (NA) of 0.8. The scan speed was set at 400 Hz (Hz). The microscope pinhole was set at 0.064 mm and the average size depth of images was between 65 and 70 µm; the average number of sections per image was 25. The image format was 1024 × 1024 pixels, 8 bits per sample and 1 sample per pixel.CLSM Subcellular localization of H2O2 and active peroxidases using 10-acetyl-3,7-dihydroxyphenoxazine (Amplex Red)B. nigra leaves from rooted potted plants were treated with 50 µl of either 50 or 100 ppm of (Z)-11-16:Ald (Table S2) after incubation with the dye 10-acetyl-3,7-dihydroxyphenoxazine (Amplex Red) as described earlier22. The Molecular Probes Amplex Red Hydrogen Peroxide/Peroxidase Assay kit (A-22188) was used and dissolved in MES-Na buffer 50 mM (pH6.0) containing 0.5 mM calcium sulfate to obtain a 50 μM solution. Leaves where then mounted on a Leica TCS SP2 miscroscope as described above. Scannings were recorded after 180 min using the HCX PL APO 63x/1.20 W Corr/0.17CS objective. The microscope was operated with a Laser Ar (458 nm/5 mW; 476 nm/5 mW; 488 nm/20 mW; 514 nm/20 mW); a Laser HeNe 543 nm/1,2 mW and a Laser HeNe 633 nm/10 mW.ROS-scavenging enzyme activities and soluble protein determinationLeaves were collected immediately after 30 min of exposure to either 100 ppm of (Z)-11-16:Ald or control (Table S2). Intact leaves of two pooled plants were frozen in liquid N2 and stored at -80ºC before enzyme extraction. Frozen leaves were used for extraction of ROS scavenger enzymes following the method described in Maffei et al.22. All steps were carried out at 4 °C. Plant material was ground with a mortar and pestle under liquid nitrogen in cold 50 mM sodium phosphate buffer, pH 7.5, containing 250 mM sucrose, 1.0 mM EDTA, 10 mM KCl, 1 mM MgCl2, 0.5 mM phenylmethylsulfonyl fluoride (PMSF), 0.1 mM dithiothreitol (DTT), and 1% (w/v) polyvinylpolypyrrolidone (PVPP) in a 1:10 proportion (weight of plant material to buffer volume). The homogenate was then centrifuged at 25,000 g for 20 min at 4 °C and the supernatant was used directly for measurement of enzyme activity. The soluble protein concentration was measured using the method established by Bradford46 using bovine serum albumin as a standard.Catalase (CAT) activity was assayed spectrophotometrically by monitoring the absorbance change at 240 nm due to the decreased absorption of H2O2 (ɛ = 39.4 mM−1 cm−1). The reaction mixture in 1 mL final volume contained 50 mM Na-P, pH 7.0, 15 mM H2O2, and the enzyme extract. The reaction was initiated by addition of H2O2.Peroxidase (POX) activity was measured by detecting the oxidation of guaiacol (ɛ = 26.6 mM−1 cm−1) in the presence of H2O2. The reaction mixture contained 50 mM Na-P, pH 7.0, 0.33 mM guaiacol, 0.27 mM H2O2, and the enzyme extract in a 1.0 mL final volume. The reaction was started by addition of guaiacol and measured spectrophotometrically at 470 nm.Superoxide dismutase (SOD) activity was measured by reduction of nitro blue tetrazolium due to a photochemically generated superoxide anion. One ml of assay mixture consisted of 50 mM Na-P buffer, pH 7.8, 13 mM methionine, 75 μM nitro blue tetrazolium (NBT), 2 μM riboflavin, 0.1 mM EDTA, and the enzyme extract. Riboflavin was added as the last reagent. Samples were placed 30 cm below a light source (60 µmol m−1 s−1), and the reaction was allowed to run for 15 min. The reaction was stopped by switching off the light. A non irradiated reaction mixture, which was run in parallel, did not develop colour and served as a control. The absorbance was read at 560 nm.Quantitative gene expression analysis by Real-time PCRTotal RNA was isolated from control or treatment leaf tissues using RNA Isolation mini Kit (Machery-Nagel, Germany), and RNase- Free DNase according to the manufacturer’s protocols. The quality of RNA was checked in 1% agarose gel and the final yield was checked with a Spectrophotometer (Pharmacia Biotech Ultrospec 3000, United States). The cDNA synthesis was performed starting from 1 µg RNA using the High Capacity cDNA Reverse Transcription kit (Applied Biosystem, United States). Primers for real-time PCR were designed using the Primer 3.0 software47 and the relative sequences are listed in Supplementary Table S3. The real-time PCR was performed on an Mx3000P Real-Time System (Agilent Technologies, United States) using SYBR green I with the dye ROX as an internal loading standard. The reaction mixture was 10 µl in volume and comprised 5 µl of 2 × Maxima SYBR Green qPCR Master Mix (Thermo Fisher Scientific), 0.5 ml of cDNA, and 100 nM of primers (Integrated DNA Technologies, United States). The thermal conditions were as follows: 10 min at 95 °C, 40 cycles of 15 s at 95 °C, 20 s at 57 °C, and 30 s at 72 °C. Fluorescence was read after each annealing and extension phase. All runs were followed by a melting curve analysis from 55 to 95 °C. Two reference genes, ACT1 and eEF1Balpha2, were used to normalize the results. The sequences of the primers used in this work for CAT1, CuZnSOD1, PER4, ACT1 and eEF1Balpha2 are reported in Table S3. All amplification plots were analyzed with the MX3000P software (Agilent Technologies, United States) to obtain Ct values. Real-time PCR data are expressed as fold change of the treatment with respect to the control.Statistical analysisArea consumed by larvae, Vm measurements, enzyme activity and gene expression data were analysed using SPSS 25 software (IBM Corp. Armonk, USA). The normality of data and homogeneity of variances were checked and log transformed when the data did not meet assumptions for parametric analyses. Because we observed no significant differences between the control and the solvent control, we directly compared the control with (Z)-11-16:Ald for all analyses. Differences between treatments were analysed using T-tests for the fed area, gene expression and enzyme activity. Volatile emission rates were log transformed and auto-scaled (mean-centered and divided by the standard deviation of each variable). Partial Least Squares – Discriminant Analysis (PLS-DA) was performed on emission rates with the R software (v. 3.4.3) with the package vegan and RVAideMemoire with cross validation based on 50 submodels (fivefold outer loop and fourfold inner loop). A pairwise test was performed, based on PLS-DA with 999 permutations, to highlight the differences between treatments. The PLS-DA graphics were done with metaboanalyst (https://www.metaboanalyst.ca/). More

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