J Syst Evol

10 January 2019, Volume 57 Issue 1

Cover illustration: Upper left: Passiflora serratifolia. Lower left: Phylogenetic distribution of plastome rearrangements. Upper right: P. edulis. Middle right: Whole genome alignment of Passiflora plastomes. Lower right: P. nitida. Photographs by Lawrence E. Gilbert. Designed by Alice Tangerini. See Rabah et al., pp. 1–14 in this issue.

Research Articles

Passiflora plastome sequencing reveals widespread genomic rearrangements

Samar O. Rabah, Bikash Shrestha, Nahid H. Hajrah, Mumdooh J. Sabir, Hesham F. Alharby, Mernan J. Sabir, Alawiah M. Alhebshi, Jamal S. M. Sabir, Lawrence E. Gilbert, Tracey A. Ruhlman, and Robert K. Jansen

J Syst Evol. 2019, 57(1): 1-14.
https://doi.org/10.1111/jse.12425

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Although past studies have included Passiflora among angiosperm lineages with highly rearranged plastid genomes (plastomes), knowledge about plastome organization in the genus is limited. So far only one draft and one complete plastome have been published. Expanded sampling of Passiflora plastomes is needed to understand the extent of the genomic rearrangement in the genus, which is also unusual in having biparental plastid inheritance and plastome‐genome incompatibility. We sequenced 15 Passiflora plastomes using either Illumina paired‐end or shotgun cloning and Sanger sequencing approaches. Assembled plastomes were annotated using Dual Organellar GenoMe Annotator (DOGMA) and tRNAscan‐SE. The Populus trichocarpa plastome was used as a reference to estimate genomic rearrangements in Passiflora by performing whole genome alignment in progressiveMauve. The phylogenetic distribution of rearrangements was plotted on the maximum likelihood tree generated from 64 plastid encoded protein genes. Inverted repeat (IR) expansion/contraction and loss of the two largest hypothetical open reading frames, ycf1 and ycf2, account for most plastome size variation, which ranges from 139 262 base pairs (bp) in P. biflora to 161 494 bp in P. pittieri. Passiflora plastomes have experienced numerous inversions, gene and intron losses along with multiple independent IR expansions and contractions resulting in a distinct organization in each of the three subgenera examined. Each Passiflora subgenus has a unique plastome structure in terms of gene content, order and size. The phylogenetic distribution of rearrangements shows that Passiflora has experienced widespread genomic changes, suggesting that such events may not be reliable phylogenetic markers.
Molecular markers for phylogenetic applications derived from comparative plastome analysis of Prunus species

Hyoung Tae Kim, Jung Sung Kim, You Mi Lee, Jeong-Hwan Mun, and Joo-Hwan Kim

J Syst Evol. 2019, 57(1): 15-22.
https://doi.org/10.1111/jse.12453

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Interspecific and intergeneric relationships of Prunus s.l. are still unclear due to low levels of genetic variation among species, and resulting partially unresolved phylogenetic inferences. Here we sequenced and compared six complete plastomes from two subgenera of Prunus in order to choose molecular markers to increase the amount of genetic variation suitable for inference of Prunus phylogeny. The plastomes range between 157 817 and 158 995 bp in length, and we found different levels of inverted repeat (IR) contraction among the three sampled subgenera of Prunus s.l. Most regions in Prunus plastomes considered individually provide low phylogenetic resolution at the subgenus or species level compared to a tree constructed using all 78 coding regions combined. We compared levels of variation among 206 coding regions and noncoding (intergenic and intron) plastid regions and inferred phylogenies from each region considered individually. We then chose using two regions together for future studies of relationships in Prunus, ycf1 and trnT-L, that display high to moderate levels of variation among coding and intergenic regions, respectively, and that individually permit inference of resolved species-level trees in Prunus with moderate to strong branch support. Considered together, these two regions allow inference of the same topology of Prunus inferred using all coding plastid regions combined, with comparable levels of tree support to the full plastome set. These two loci should therefore be useful as a plastid phylogenetic marker set for further inference of relationships within Prunus s.l.
Discovery of the genus Pseudoroegneria (Triticeae, Poaceae) in the Western Mediterranean on exploring the generic boundaries of Elymus

Víctor Lucía, M. Montserrat Martínez-Ortega, Enrique Rico, and Kesara Anamthawat-Jónsson

J Syst Evol. 2019, 57(1): 23-41.
https://doi.org/10.1111/jse.12426

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In this study, we review the classification of two species, Elymus hispanicus and E. marginatus, which are restricted to highly valuable and sensitive Mediterranean ecosystems. The genomic composition of the two species is analysed by in situ hybridization. In addition, lodicule morphology and foliar anatomy of both species are compared with those of E. caninus, E. repens, E. sibiricus (i.e., the type species of Elymus s.s.) and Pseudoroegneria strigosa (i.e., the type species of Pseudoroegneria). The genomic formula 2n = 8x = 56; HStStSt is proposed for E. hispanicus and 2n = 4x = 28; StSt for E. marginatus. In this latter species, the absence of the ribosomal genes in one of the two St genomes suggests that diploidization may have occurred during the evolution the species. Regarding foliar anatomy, E. hispanicus, E. caninus, E. repens, and E. sibiricus shared several characteristics, but the leaf blades of E. marginatus proved anatomically more similar to those of Ps. strigosa. The data compiled support the contention that: (1) E. hispanicus belongs to Elymus s.s.; (2) E. marginatus should be transferred to Pseudoroegneria; and (3) the morphology of the lodicules should be carefully reconsidered for appropriately describing the boundaries between Elymus s.s. and Pseudoroegneria. The new combination Ps. marginata is proposed and a detailed iconography of the plant is provided.
Advances in the systematics and evolution of western Mediterranean representative species of the Pentanema conyzae clade through genetic fingerprinting

David Gutiérrez-Larruscain, Santiago Andrés-Sánchez, Enrique Rico, and María Montserrat Martínez-Ortega

J Syst Evol. 2019, 57(1): 42-54.
https://doi.org/10.1111/jse.12431

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Forty-five populations of Pentanema corresponding to seven species included in the Pentanema conyzae clade have been studied using AFLP fingerprinting. The results show that allopolyploidization could have been involved in the diversification of this group, specifically in species P. langeanum and P. maletii. Molecular data confirm the presence of P. britannicum in the Iberian Peninsula and key steps are provided to identify the species that are morphologically the most challenging.
Comparative genomics of figworts (Scrophularia, Scrophulariaceae), with implications for the evolution of Scrophularia and Lamiales

Wu-Qin Xu, Jocelyn Losh, Chuan Chen, Pan Li, Rui-Hong Wang, Yun-Peng Zhao, Ying-Xiong Qiu, Cheng-Xin Fu

J Syst Evol. 2019, 57(1): 55-65.
https://doi.org/10.1111/jse.12421

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The figwort genus Scrophularia L. (Scrophulariaceae) comprises 200–300 species and is widespread throughout the temperate Northern Hemisphere. Due to reticulate evolution resulting from hybridization and polyploidization, the taxonomy and phylogeny of Scrophularia is notoriously challenging. Here we report the complete chloroplast (cp) genome sequences of S. henryi Hemsl. and S. dentata Royle ex Benth. and compare them with those of S. takesimensis Nakai and S. buergeriana Miq. The Scrophularia cp genomes ranged from 152 425 to 153 631 bp in length. Each cp genome contained 113 unigenes, consisting of 78 protein‐coding genes, 31 transfer RNA genes, and 4 ribosomal RNA genes. Gene order, gene content, AT content and IR/SC boundary structure were nearly identical among them. Nine cpDNA markers (trnH‐psbA, rps15, rps18‐rpl20, rpl32‐trnL, trnS‐trnG, ycf15‐trnL, rps4‐trnT, ndhF‐rpl32, and rps16‐trnQ) with more than 2% variable sites were identified. Our phylogenetic analyses including 55 genera from Lamiales strongly supported a sister relationship between ((Bignoniaceae + Verbenaceae) + Pedaliaceae) and (Acanthaceae + Lentibulariaceae). Within Scrophulariaceae, a topology of (S. dentata + (S. takesimensis + (S. buergeriana + S. henryi))) was strongly supported. The crown age of Lamiales was estimated to be 85.1 Ma (95% highest posterior density, 70.6–99.8 Ma). The higher core Lamiales originated at 65.6 Ma (95% highest posterior density, 51.4–79.4 Ma), with a subsequent radiation that occurred in the Paleocene (between 55.4 and 62.3 Ma) and gave birth to the diversified families. Our study provides a robust phylogeny and a temporal framework for further investigation of the evolution of Lamiales.
Enhanced genetic diversity of weedy rice populations associated with latitude decreases revealed by simple sequence repeat fingerprints

Zhe Wang, Min-Jie Fu, Hai-Ge Zhu, Yue Zhu, Xiang-Xiang Zhao, and Bao-Rong Lu

J Syst Evol. 2019, 57(1): 66-74.
https://doi.org/10.1111/jse.12428

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Weedy rice (WR, Oryza sativa L. f. spontanea) is a noxious agricultural weed, infesting rice fields worldwide and causing tremendous yield losses of cultivated rice. However, little is known about the relationship between genetic diversity and distribution of WR populations across a wide latitudinal gradient, in addition to its reasons for genetic differentiation. To determine the distribution of genetic diversity and differentiation, we analyzed 20 WR populations collected from wide geographic ranges of rice-planting regions across Northeast, Jiangsu and Guangdong provinces of China, and Sri Lanka, based on 20 simple sequence repeat loci. Our results indicated a significant negative correlation (R = 0.84, P < 0.01) between genetic diversity and latitudinal locations of WR populations. The Mantel test (R² = 0.49, P < 0.01) showed distinct groupings of WR populations from different rice-planting regions, fitting an isolation-by-distance pattern. In addition, the STRUCTURE analysis and principal coordinates (PCoA) analysis indicated considerable genetic differentiation of WR from different rice-planting regions, which was associated with the types of co-occurring rice cultivars. We conclude based on the above results that WR genetic diversity is affected by the latitudes where WR populations are located. The genetic differentiation of WR populations is determined by their spatial distances and co-occurring rice cultivars. Such a pattern of genetic diversity and differentiation across different regions may facilitate the design of effective WR control, in addition to understanding adaptive evolution of this weed.
Resurrection of the East Asian genus Eremotropa (Monotropoideae, Ericaceae), based on molecular and morphological data

Qian-Ru Zhao, Jing Zhou, Hua Peng, and Zhen-Wen Liu

J Syst Evol. 2019, 57(1): 75-80.
https://doi.org/10.1111/jse.12429

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The monotypic genus Eremotropa Andres (Monotropoideae, Ericaceae) is endemic to central Yunnan. It was first described by Andres in 1953, and was subsequently treated as a synonym of Monotropastrum Andres (1987); however, the phylogenetic placement of this genus has not, to date, been investigated. In this study, phylogenetic analyses were undertaken using DNA sequences from the nuclear internal transcribed spacer from all species of Monotropoideae available in GenBank. Comparative morphological studies on Eremotropa, Monotropastrum, and Monotropa L. were also carried out. The molecular phylogenetic evidence suggests that Eremotropa is sister to a clade formed by Monotropa and the remaining species of Monotropastrum, thus rendering Monotropastrum not monophyletic. Morphologically, Eremotropa differs from Monotropastrum in plant color, inflorescence type, length of the style, and size of the baccate fruit. Consequently, molecular and morphological evidence supports the resurrection of Eremotropa, which contains only one species, E. sciaphila Andres, as distinct from Monotropastrum.
Pollination in Lilium sargentiae (Liliaceae) and the first confirmation of long-tongued hawkmoths as a pollinator niche in Asia

Chang-Qiu Liu, Hang Sun

J Syst Evol. 2019, 57(1): 81-88.
https://doi.org/10.1111/jse.12419

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The geographical distribution of pollinators is an important factor determining the biogeographical pattern of floral evolution and diversification. In Africa, a guild of plant species has converged in a floral syndrome for pollination by long‐tongued hawkmoths (predominantly Agrius convolvuli). It is hypothesized that such floral convergence could track the geographical distribution of long‐tongued hawkmoths, so it may not be confined to Africa. We investigated the pollination biology of Lilium sargentiae E. H. Wilson, which is endemic to China and exhibits traits suggestive of long‐tongued hawkmoth pollination. Lilium sargentiae was visited by A. convolvuli as well as small beetles (Nitidulidae) but pollination was mostly or totally effected by the moth. It was consistent with other hawkmoth‐pollinated plants in terms of floral tube length, nectar traits, tepal reflectance, and scent composition. We present the first experimental evidence for the hypothesis proposed above and for hawkmoth pollination in the widespread and ornamentally and economically important genus Lilium L. in a natural habitat. Our findings imply that long‐tongued hawkmoths (especially the extremely widespread A. convolvuli) as a distinctive pollinator niche may have underlain the evolution of long‐tubed (>8 cm) flowers across different continents.

List of Reviewers

List of Reviewers

J Syst Evol. 2019, 57(1): 89-90.
https://doi.org/10.1111/jse.12477

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The Journal of Systematics and Evolution would like to acknowledge and thank the following reviewers for their contributions in the period January 1–December 31 in 2018:

Alexander, Jason

Álvarez Fernández, Inés

Appelhans, Marc

Assadi, Mostafa

Barkman, Todd

Bauret, Lucie

Bayer, Randall J

Bell, Charles

Bergholz, Kolja

Bernardello, Gabriel

Bippus, Alex

Blackmore, Stephen

Bocksberger, Gaelle

Boufford, David E.

Bruneau, Anne

Cai, Xing‐Xing

Cevallos, Sergio

Chen, Zhi‐Duan

Clement, Wendy

Cohen, James

Comes, Peter

Crayn, Darren

Crespo, Manuel B.

Da Cunha, Maura

De‐Nova, J.

Deng, Yun‐Fei

Dong, Shi‐Yong

Dong, Wen‐Pan

Duan, Yuan‐Wen

Estrada‐Ruiz, Emilio

Fan, Xing

Fatoretto, Julio

Feldberg, Kathrin

Feliner, Gonzalo

Fiaschi, Pedro

Freire, Susana

Freyman, Will

Gao, Lian‐Ming

Garnatje, Teresa

German, Dmitry A.

Gernandt, David

Gerrath, Jean

Gillespie, Emily

Gong, Xun

Graham, Alan

Grote, Paul

Gu, Hong‐Ya

Gu, Xingyou

Guo, Yan‐Ping

Guo, Zhen‐Hua

Harbert, Robert

Harris, AJ

Hartman, Ronald

Hearn, David

Herrera, Fabiany

Hodel, Richard

Hu, Zhong‐Li

Huang, Jian

Huang, Jin‐Ling

Huang, Shuang‐Quan

Ickert‐Bond, Stefanie

Jha, Sumita

Jimenez, Pedro

Jin, Jian‐Hua

Jin, Xiao‐Hua

John, MacDougal

Johnson, Leigh

Jud, Nathan

Kazempour‐Osaloo, Shahrokh

Keeley, Sterling

Keppel, Gunnar

Kikvidze, Zaal

Kilian, Norbert

Kim, Ki‐Joong

Kong, Hang‐Hui

Kunzmann, Lutz

Kwembeya, Ezekiel G.

Li, Hong‐Tao

Li, Huang

Li, Jianhua

Li, Lin‐Feng

Li, Rong

Li, Zhong‐Hu

Liang, Liang

Liao, Wan‐Jin

Liu, Jian‐Quan

Liu, Jie

Liu, Xiao‐Yan

Lombardi, Julio Antonio

Lu, Li‐Min

Lu, Zhi‐Qiang

Ma, Jian‐Chao

Ma, Xiao

Ma, Xiao‐Fei

Manchester, Steven

Mao, Kang‐Shan

Marhold, Karol

Maurin, Olivier

McAllister, Hugh

Metzgar, Jordan

Meyer, Herbert

Michael, Möller

Michelangeli, Fabian A.

Mishler, Brent

Momohara, Arata

Morales‐Briones, Diego F.

Morrone, Juan José

Nakajima, Jimi

Nauheimer, Lars

Nie, Ze‐Long

Nowak, Michael

Olsen, Kenneth M.

Ornelas, Juan Francisco

Patel, Nikisha

Paun, Ovidiu

Peralta, Denilson F.

Pirie, Michael

Qi, Zhe‐Chen

Qiang, Sheng

Qiu, Ying‐Xiong

Ran, Jin‐Hua

Reagon, Micheal

Reginato, Marcelo

Rojas‐Andrés, Blanca

Rong, Jun

Rubin, Matthew J.

Salazar‐Mendias, Carlos

Salino, Alexandre

Sanchez‐Puerta, Virginia

Scherson, Rosa

Schwarz Taylor, Erika

Sessa, Emily

Shan, Hong‐Yan

Shi, Gong‐Le

Shi, Su‐Hua

Simpson, Michael

Soejima, Akiko

Song, Bao‐Hua

Spalink, Daniel

Španiel, Stanislav

Stevens, Peter

Stone, Robert

Strijk, Joeri

Su, Tao

Su, Xu

Sun, Bai‐Nian

Sun, Hai‐Qin

Sun, Hang

Sun, Yan‐Xia

Tank, David

Thomas, Daniel

Tomescu, Alexandru

Uncu, Ayse

Vargas, Pablo

Vatanparast, Mohammad

Vorontsova, Maria S.

Wang, Hong‐Fang

Wang, Jian‐Bo

Wang, Wei

Wen, Jun

Wheeler, Elisabeth

Wilson, Barbara

Wilson, Peter

Wolfe, Andrea

Xia, Hui

Xiao, Sha

Xie, Lei

Yan, Yue‐Hong

Yang, Chun‐Feng

Yang, Shi‐Xiong

Yang, Yong‐Ping

Yu, Wen‐Bin

Yu, Yan

Yue, Ji‐Pei

Zarco, Carlos Romero

Zhang, Jian

Zhang, Ti‐Cao

Zhang, Wenheng

Zhang, Wen‐Ju

Zhao, Gui‐Fang

Zhao, Ting‐Ting

Zhou, Ren‐Chao

Zhou, Shi‐Liang

Zhou, Yong‐Hong

Zhou, Yong‐Feng

Zhou, Zhe‐Kun

Zhou, Zhuo

Zimmer, Elizabeth