Guo et al. BMC Genomics (2018) 19:392 https://doi.org/10.1186/s12864-018-4784-9 RESEARCH ARTICLE Open Access Comparative transcriptome analysis of the invasive weed Mikania micrantha with its native congeners provides insights into genetic basis underlying successful invasion Wuxia Guo1, Ying Liu1, Wei Lun Ng1, Pei-Chun Liao2, Bing-Hong Huang2, Weixi Li1, Chunmei Li1, Xianggang Shi1 and Yelin Huang1* Abstract Background: Mikania micrantha H.B.K. (Asteraceae) is one of the world’s most invasive weeds which has been rapidly expanding in tropical Asia, including China, while its close relative M. cordata, the only Mikania species native to China, shows no harm to the local ecosystems. These two species are very similar in morphology but differ remarkably in several ecological and physiological traits, representing an ideal system for comparative analysis to investigate the genetic basis underlying invasion success. In this study, we performed RNA-sequencing on the invader M. micrantha and its native congener M. cordata in China, to unravel the genetic basis underlying the strong invasiveness of M. micrantha. For a more robust comparison, another non-invasive congener M. cordifolia was also sequenced and compared. Results: A total of 52,179, 55,835, and 52,983 unigenes were obtained for M. micrantha, M. cordata,andM. cordifolia, respectively. Phylogenetic analyses and divergence time dating revealed a relatively recent split between M. micrantha and M. cordata, i.e., approximately 4.81 million years ago (MYA), after their divergence with M. cordifolia (8.70 MYA). Gene ontology classifications, pathway assignments and differential expression analysis revealed higher representation or significant up-regulation of genes associated with photosynthesis, energy metabolism, protein modification and stress response in M. micrantha than in M. cordata or M. cordifolia. Analysis of accelerated evolution and positive selection also suggested the importance of these related genes and processes to the adaptability and invasiveness of M. micrantha. Particularly, most (77 out of 112, i.e. 68.75%) positively selected genes found in M. micrantha could be classified into four groups, i.e., energy acquisition and utilization (10 genes), growth and reproduction (13 genes), protection and repair (34 genes), and signal transduction and expression regulation (20 genes), which may have contributed to the high adaptability of M. micrantha to various new environments and the capability to occupy a wider niche, reflected in its high invasiveness. Conclusions: We characterized the transcriptomes of the invasive species M. micrantha and its non-invasive congeners, M. cordata and M. cordifolia. A comparison of their transcriptomes provided insights into the genetic basis of the high invasiveness of M. micrantha. Keywords: Invasion, Eco-adaptation, Positive selection, Comparative transcriptomics, Mikania * Correspondence: [email protected] 1State Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-sen University, 135 Xingang West Road, 510275 Guangzhou, Guangdong, People’s Republic of China Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Guo et al. BMC Genomics (2018) 19:392 Page 2 of 17 Background 1884 in Hong Kong, and after then, M. micrantha has When a species is introduced into a new environment, it expanded in southern China, covering Hong Kong and either does not adapt and quickly goes extinct or persists the Guangdong and Taiwan provinces [33]. In contrast, and establishes in the new environment. Species that live M. cordata is the only Mikania species native in South on may become competitive and colonize new areas and China, distributed in Yunnan, Hainan, and Taiwan niches at high rates, eventually becoming successful in- provinces [13, 34, 35]. Interestingly, although M. micrantha vaders. Since many invasive species pose serious threat and M. cordata appear to be quite similar to each other in to native biodiversity and cause severe economic loss in morphology and life style, they show considerable differ- the affected regions [1–5], biological invasion has long ences in many ecological traits, such as niche requirements, been recognized as a leading threat to the functioning of eco-adaptability, and most importantly, invasiveness. As ob- local ecosystems and global biodiversity [6, 7]. As trans- served in Taiwan where they co-exist, for example, while mission of biological material increases worldwide due M. micrantha run rampant and becomes a major pest of to the development of international trade and more fre- crops and forests [36, 37], M. cordata grows slowly and quent human activity [5, 8], such crisis becomes increas- exhibits no harm to other native species and the local ingly severe. Understanding the mechanisms by which ecosystems [38]. invasive plants succeed would eventually be useful for Previous studies on the invasion of M. micrantha were control efforts [9] and thus are of great importance and mainly performed on the species alone and/or focused on necessity. Over the past decades, extensive insights have its ecological impacts and physiological traits [9, 35, 39–49]. been gained on the biology or ecology of plant invasion, Comparisons between M. micrantha and its non-invasive which suggests several factors to be responsible for inva- congeners that share morphological and life-history traits is sive success, including external environmental conditions lacking [9, 38, 46, 47]. Among the few comparative studies, (e.g., lack of natural enemies, increased anthropogenic dis- one of the most compelling observations is the higher turbance, and a wide range of invasive habitats) and their photosynthetic efficiency and capability of acclimation intrinsic biological characteristics (e.g., the capability of to light observed in M. micrantha compared to M. cor- rapid reproduction, broad eco-adaptability, and strong data [9, 24, 28, 47], which is considered to be at least allelopathic effects) [10–15]. However, the relative lack partly associated with the invasiveness of M. micrantha. of genomic data for invasive plants, which represent Studies on habitat preferences have revealed that M. mostly non-model species, hinders research on this micrantha can invade a relatively wider light niche, group of organisms at the molecular level. As the devel- while M. cordata can only tolerate shady environments opment of transcriptome sequencing technology offers in tropical and subtropical China [9, 38, 47, 50, 51]. M. a convenient and efficient means to obtain genome re- micrantha has also been found to be able to achieve ex- sources in non-model species [16–18], it provides an tremely fast growth and reproduction in new environ- opportunity for comparative study of closely related in- ments [52], hinting that efficient response to new abiotic vasive and non-invasive congeners, as an effective ap- and biotic stresses, such as climate, soils, and pathogens proach to identify the genetic basis and mechanisms of [53, 54] followed by successful adaptation and range ex- invasive success [9, 19, 20]. pansion, could be another remedy for its invasiveness. Yang Mikania micrantha H.B.K. is a perennial vine that be- et al. (2017) has also preliminarily associated the ecological longs to the family Asteraceae. This species is native to adaptation of M. micrantha to different habitats with dif- tropical America, and has been recognized as one of the ferential expression of genes involved in high light intensity world’s most notorious invaders [9, 21]. With its extremely stress response, protein folding, and oxidative processes by fast growth and ability of both sexual and asexual comparing native and introduced M. micrantha popula- reproduction, M. micrantha can rapidly colonize disturbed tions [49]. While Huang et al. (2012) also provided a pre- habitats, while competing with the native vegetation and liminary insight of the M. micrantha transcriptome, retarding their growth [5, 22–24]. Due to both external constrained by the sequencing technology and bioinfor- (e.g., human activity) and internal (e.g., strong invasiveness) matics tools developed then, the size and quality of data reasons, the plant is now widely distributed across tropical obtained at that time was relatively limited for a thorough Asia and the Pacific Islands, causing serious economic and study [55]. Although these studies have undoubtedly ex- environmental impacts [5, 13, 21, 25–29]. Among the tended our understanding on the invasiveness of M. more than 400 Mikania species, most of which native to micrantha from the physiological and ecological perspec- tropical America, M. micrantha istheonlyspeciesthathas tives (i.e., the physiological plasticity and rapid adaptive spread from the New World to the Old World, and now regulation), the underlying molecular mechanisms remains coexists with its native