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Taxonomy of Duckweeds (Lemnaceae), Potential New Crop Plants

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Taxonomy of Duckweeds (Lemnaceae), Potential New Crop Plants Emirates Journal of Food and Agriculture. 2016. 28(5): 291-302 doi: 10.9755/ejfa.2016-01-038 http://www.ejfa.me/ REVIEW ARTICLE Taxonomy of duckweeds (Lemnaceae), potential new crop plants K. Sowjanya Sree1, Manuela Bog2, Klaus-Juergen Appenroth3* 1Amity Institute of Biotechnology, Amity University Uttar Pradesh, Noida, India, 2University of Regensburg, Institute of Plant Sciences, Regensburg, Germany, 3Institute of General Botany and Plant Physiology, University of Jena, Jena, Germany ABSTRACT Duckweeds are increasingly gaining interest because of their potential as a new aquaculture crop. In the present era of high through- put research, duckweed taxonomy has to be emphasized in order to support and strengthen scientific communication and commercial application. Since the publication of the fundamental monograph on Lemnaceae by E. Landolt in 1986, a number of changes have taken place in terms of their taxonomic position and nomenclature, which we summarize in this review. We report here about the systematic position of this plant family and the changes in its organization. Three additional species were identified; one new genus and subsequently one of the species was re-defined after the publication of the key of determination in 1986. At present Lemnaceae comprises of 37 species grouped into five genera. We envisage that this review will serve as a compilation of all these recent revisions, describing the state of art of duckweed systematics. Keywords: Aquaculture; Duckweed; Lemnaceae; Taxonomy; Crop plant INTRODUCTION Appenroth, 2014; Sree et al., 2015a, b) can be used as a raw material for biofuel and biogas plants (Jain et al., The present “blooming era” of “resurgence of duckweed 1992; Su et al., 2014; Cui and Cheng, 2015). This would research and applications” (Zhao et al., 2012; Lam et substantially replace the use of food crops that are grown al., 2014; Appenroth et al., 2015b) is based mainly on in arable lands as raw materials for biofuel production. their high potential for practical application. Lemnaceae Taken together, plants of this family have the potential comprises one of the fastest growing angiosperms as new crop plants. (Sree et al., 2015c; Ziegler et al., 2015). In some Asian countries, duckweeds have been used for human nutrition Duckweeds, monocotyledonous aquatic plants, are for generations (Bhanthumnavin and McGarry, 1971; cf. represented by 37 species (Appenroth et al., 2013). This van der Spiegel et al., 2013), because of their high protein number is often cited incorrectly probably because of the content (Appenroth et al., 1982; Cheng and Stomp, following reason. In the year 2000, it became clear that 2009). Duckweeds have the potential to replace soya Lemna ecuadoriensis is a synonym of L. obscura (Austin) Daubs bean products at least partially as a source of protein. (Landolt, 2000). But by mistake (personal correspondence As demonstrated by several projects, duckweeds proved to KJA), this merger was not considered in Les et al. (2002) to be advantageous when fed to domesticated animals and also not in Tippery et al. (2015). As a result, the total e.g., cattle, sheep, horses, rabbits (reviews in Landolt number of duckweed species was mentioned as 38 instead and Kandeler, 1987; Cheng and Stomp, 2009), poultry of 37, creating confusion to the readers. The 37 species are and water fowls (Muztar et al., 1979; Anderson et al., categorized into five well-defined generaFig ( . 1, Table 1): 2011), fish (Hassan and Edwards, 1992; Pipalova, 2003), Spirodela (2 species), Landoltia (1), Lemna (13), Wolffiella (10) and pigs (Van et al., 1997). Apart from their use as food and Wolffia (11) (Appenroth et al., 2013). These aquatic and feed, duckweed biomass with high starch content angiosperms are cosmopolitan in distribution except for produced under suitable cultivation conditions (Sree and some endemic species (Landolt, 1986). *Corresponding author: Klaus-Juergen Appenroth, Institute of General Botany and Plant Physiology, University of Jena, Dornburger Str. 159, 07743 Jena, Germany. E-mail: [email protected] Received: 13 January 2016; Revised: 14 March 2016; Accepted: 15 March 2016; Published Online: 25 March 2016 Emir. J. Food Agric ● Vol 28 ● Issue 5 ● 2016 291 Sree, et al.: Taxonomy of Lemnaceae Table 1: Presently accepted genera and species of the plant family Lemnaceae Dumort Subfamily Genera Species Lemnoideae Spirodela S. polyrhiza (L.) Schleid. Engl. Schleid. S. intermedia W.Koch Landoltia L. punctata (G.Mey.) Les & D.J.Crawford Les & Crawford Lemna L. L. disperma Hegelm. L. gibba L. L. japonica Landolt L. minor L. L. obscura (Austin) Daubs L. turionifera Landolt L. trisulca L. L. aequinoctialis Welw. Fig 1. Internal structure of the family: Lemnaceae. The relation of L. perpusilla Torr. genera and subfamilies based on Les et al. (2002) and Tippery et al. L. tenera Kurz (2015). L. minuta Kunth L. valdiviana Phil. Elias Landolt from ETH Zurich, Switzerland has collected L. yungensis Landolt duckweeds from all over the world since the mid-1950s Wolffioideae Wolffiella W. caudata Landolt and established a duckweed stock collection (Landolt, Engl. Hegelm. 1957; Appenroth et al., 2015a) which originally exceeded W. denticulata (Hegelm.) Hegelm. W. gladiata (Hegelm.) Hegelm. one thousand clones. Based mainly on morphological W. lingulata (Hegelm.) Hegelm. investigations, he published a “key of determination” W. neotropica Landolt of duckweeds (Landolt, 1980) which was later slightly W. oblonga (Phil.) Hegelm. modified in the first part of his famous monograph W. welwitschii (Hegelm.) Monod (Landolt, 1986). Within the last three decades, quite a W. rotunda Landolt number of changes have been introduced to taxonomic W. hyalina (Delile) Monod classification of duckweeds in comparison to the published W. repanda (Hegelm.) Monod Wolffia W. angusta Landolt key. Moreover, molecular taxonomy and barcoding of Horkel ex duckweed species (Wang et al., 2010; Bog et al., 2010, 2013, Schleid. 2015; Borisjuk et al., 2015) has made huge progress and it W. arrhiza (L.) Horkel ex Wimm. aids in identification of duckweed species. However, it is W. columbiana H.Karst. not practically and economically viable to determine each W. cylindracea Hegelm. W. elongata Landolt of the collected duckweed clones by Amplified Fragment W. globosa (Roxb.) Hartog & Plas Length Polymorphism (AFLP) or by sequencing of DNA W. neglecta Landolt markers. Therefore, determination of duckweed species W. australiana (Benth.) Hartog & Plas based on their morphology remains crucial for their W. borealis (Engelm. ex Hegelm.) Landolt identification. An update to the “key of determination” of W. brasiliensis Wedd. all the duckweed species known to date is a prerequisite to W. microscopica (Griff.) Kurz facilitate accuracy in communication amongst researchers in academia and industry, and also entrepreneurs in this Taxonomic position of the family Lemnaceae field, especially keeping in view the practical applications Duckweed species are monophyletic with those of the of duckweeds. Araceae (Cabrera et al., 2008; Cusimano et al., 2011). However, the branching appears to have started about In this review we discuss the taxonomic position of 104 Ma ago in the Early Cretaceous when the breakup of duckweeds and the classification changes made since the Pangea was in its final stage (Nauheimer et al., 2012). This publication of Landolt’s monograph in 1986 (Table 2). is one reason why we prefer keeping Lemnaceae as a family This revision shall help students and newcomers to the of its own (Appenroth et al., 2015a). The monophyly does field of duckweed research and applications to become not necessarily mean that duckweeds have to be integrated quickly acquainted with this expanding field and to use the into the family of Araceae and be treated as a subfamily accurate terms and nomenclature. Lemnoideae, as preferred e.g. by Nauheimer et al. (2012). 292 Emir. J. Food Agric ● Vol 28 ● Issue 5 ● 2016 Sree, et al.: Taxonomy of Lemnaceae Table 2: Newly discovered species and revised nomenclature after the publication of the duckweed monograph by Landolt (1986) S. No. Presently accepted nomenclature Old nomenclature (not valid=synonym) Reference 1 Landoltia punctata (G.Mey.) Les & D.J.Crawford Spirodela punctata Les and Crawford (1999) Spirodela oligorrhiza Spirodela sichuanensis Li and Landolt (2010) 2 Spirodela polyrhiza (L.) Schleid. Spirodela polyrrhiza Appenroth et al. (1990) 3 Lemna aequinoctialis Welw. Lemna paucicostata Landolt (1986) Lemna aoukikusa Borisjuk et al. (2015) 4 Lemna minuta Kunth Lemna minuscula Reveal (1990) 5 Lemna obscura (Austin) Daubs Lemna ecuadoriensis Landolt (2000) 6 Lemna valdiviana Phil. Lemna valdesiana Landolt (1986) 7 Wolffiella caudata Landolt New species Landolt (1992) 8 Wolffia neglecta Landolt New species Landolt (1994) 9 Wolffia cylindracea Hegelm. Newly defined Landolt (1994) One can separate the small group of Protoaraceae together taxonomic investigation of this species based on AFLP and with Lemnaceae from the “true Araceae” (as these two plastidic marker sequences (unpublished data; Bog, Sree groups are the most basal elements in this group), which and Appenroth) has been carried out recently together with results in three monophyletic plant families, i.e. true other species of the genus Wolffiella. These investigations Araceae, Lemnaceae and Protoaraceae (Appenroth further support its species identity. et al., 2015a). The following additional arguments speak in favour of designating Lemnaceae as a family
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