Possible Mechanisms of the Invasiveness of P. montana: Comparison
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Pueraria montana var. lobata is native to East Asia, and was introduced to many countries due to its potential for multiple uses. This species escaped under the management conditions soon after its introduction, and became a harmful weed species. This species has been listed in the top 100 of the world’s worst invasive alien species. P. montana stands expand quickly and threaten the native flora and fauna including microbiota. This species affects the concentration of carbon and nitrogen in soil and aquatic environments, and increases the amount of pollutants in the local atmosphere. Its infestation also causes serious economic losses on forestry and agriculture. 

  • adaptation
  • allelopathy
  • crop production
  • economic loss

1. Introduction

P. montana was shown to cause serial problems on the natural ecosystems and industry of the introduced ranges as described in the previous section. Although many researchers have investigated the invasive mechanism of the species, no review article has been made available.

2. Growth

P. montana grows quickly. Its stem growth rate was 3–20 cm per day, and 20–30 m per single growing season, and reached 63–320 m in length [6,59,60,61][1][2][3][4]. Frequent branching occurs from the nodes of the main stems and the branches, and the average number of primary and secondary branches was 15 and 18 per main stem, respectively. The total length of stems and branches was up to 360 m per m2 [6,61][1][4]. The negative effect of the long stem length on the water transport from roots to the apexes and top leaves was compensated for by the transpiration from the large leaves, large stem sapwood areas and water storage, and by the decreasing petiole hydraulic resistance and the maintenance of the high stem hydraulic conductance. These functions support the water transportation of the long stem species [62,63][5][6].
The number of leaves of the main stems, primary branches and secondary branches of P. montana grown for a single year in pot conditions was 19, 94 and 60, respectively [5][7], and the leaf area per gram of shoot biomass was 110–150 cm2 [1][8]. This species forms thick canopy layers, and its leaf area was 3.7–7.8 m2 per m2 of grand area [64][9], which is a 10- to 15-fold greater leaf area per unit stem compared to that of the mature tree species [1][8]. This species has also the ability to rapidly reorient its leaves to prevent self-shading, excess solar radiation and high temperature. This movement is caused by the turgor changes induced by the K+ flux into the cells of the pulvini at the base of the petioles of the leaves [65,66][10][11]. The leaf reorientation and thick canopy of this species enable it to effectively receive solar radiation for the photosynthesis. P. montana as a vine utilizes mechanical support by climbing on trees and other vegetations, and minimizes the investment into its own supporting tissues such as its stems and branches. This species allocates large amounts of photosynthetic fixed carbon to the leaves for the production of a great number of large leaves, and to create a thick canopy structure [5,60,67][3][7][12]. The ratio of the carbon allocation to the leaves in P. montana was estimated to be 20–28% of the total fixed carbon, whereas it was 1–2% in the mature deciduous tree species [68,69][13][14]. P. montana is deciduous, and the leaves drop in autumn or early winter [64,70][9][15]. The axillary buds start to regrow and develop new leaves and stems in the early spring, and its canopy matures rapidly [70,71][15][16]. This species took about two months from the development of its first leaf to create full canopy maturity [64][9]. Although P. montana is a perennial plant species and 15-year-old stands have been found [64[9][17],72], information on the longevity of this species has not been made available.
P. montana grows well in full sunlight conditions, and its light compensation point of photosynthesis was 43 μmol m−2 s−1 [72,73][17][18]. However, the photosynthetic rate of this species is not high compared to that of other C3 plants. Its maximum photosynthesis rate was determined to be 23 μmol m−2 s−1 under field conditions [70][15]. The net carbon dioxide assimilation was between 11 and 27 μmol m−2 s−1, and its rate was similar to that of soybean [66,74][11][19]. The thick canopy layers and leaf reorientation of P. montana as described above may be able to maximize light perception and compensate for the carbon assimilation rate to maintain its growth and development.
These observations suggest that P. montana grows quickly, and forms thick canopy layers with highly branching stems and a great number of large leaves. This species effectively utilizes solar radiation for photosynthesis with the thick canopy layers and leaf movement, and allocates large amounts of photosynthetic fixed carbon to produce a great number of leaves.

3. Reproduction

P. montana also allocates large amounts of photosynthetic fixed carbon for the generation of root systems. When the stems lie down on the soil surface, the nodes of the stems easily generate nodal roots [6,61][1][4]. About 25–45% of stem nodes occurred in the nodal roots, and 61 rooted nodes per m2 were counted [75][20]. The rooted nodes frequently detach from the mother plants within 1–3 years, and develop physiologically independent clonal plants defined as ramets [75][20]. The rooted nodes from the primary-, secondary- and higher-order branches lead to a high density of the independent ramets up to tens of thousands per hectare [14][21]. The ability to create a high density of ramets may work for this species’ reproduction. The dispersion of the rooted nodes from the population periphery via hurricanes and human activity may contribute the dispersal. The clonal rate of the 87 populations of P. montana in North America was recorded to be 80% [76][22].
P. montana develops flowers in mid- to late-summer in both hemispheres, and its fruits mature in the autumn. This species produces a low number of viable seeds relative to the number of flowers [16][23]. The possible reasons for the low number of viable seeds were considered to be the high degree of floral abscission within two days before and after flowering, and a small number of healthy seeds (5–30%) [16,77][23][24]. In addition, not all populations of P. montana flowered and produced visible seeds [16,17][23][25]. Only 6 of the 78 populations were recorded to produce viable seeds in USA [78][26]. The dispersion of the seeds occurred up to 25 m from the mother plants, but the majority of the seeds stayed within 6 m from the plants [77][24]. The seeds are possibly carried for long distances by water streams such as flood water.
The seed coats are very hard and impervious, and the scarification of the seeds increased the germination. The germination rate of the healthy seeds was 7–17% and 95–100% for the seeds without and with scarification, respectively [16,79][23][27]. The seeds were released from physical dormancy, which was caused by the seed coats, through mechanical scarification and the use of fire [16,80][23][28]. The changing temperatures, which ranged from 15 °C and 6 °C (day and night) to 35 °C and 15 °C (day and night), also increased the germination [79][27], which may indicate that the germination increased with the temperature increase from spring to summer. No seedlings emerged when the seeds were exposed to flooding for more than 7 days [79][27]. Only less than 10% of the seeds were reported to germinate and establish the seedling stage due to fungal diseases and insect predation under field conditions [77][24]. Since the seeds were covered by hard and impervious coats, the seeds can establish a seed bank. However, there has been no information made available on the longevity of P. montana seeds in the soil.

4. Adaptation

P. montana thrives in areas such as forest margins, shrub areas, hill slopes, banks of water bodies, along the roads and railways, agricultural fields and disturbed lands [3,4,9,11,22][29][30][31][32][33]. This species was recorded to grow in mountainous areas up to 1200 in Japan and 1500 m in China [81,82][34][35]. It is also abundant in small islands, which have ecosystems that are very vulnerable to alien species [14,83][21][36]. This species grows well on fertile well-drained deep loamy soils with weak acidic (pH 4.5) to neutral (pH 7.0) conditions, but it can grow on many types of soils, including sandy and clay soils with a pH ranging from 3 to 8, and shallow and nutrient poor soils [16,22,23,82,84][23][33][35][37][38]. A total of 95% of fixed nitrogen via symbiosis with rhizobia was estimated to be supplied to the leaves when P. montana was grown in poor soil conditions [41][39]. Thus, the nitrogen-fixing ability of this species may contribute to its growth in poor soils. This species required an annual precipitation of 1000–15,000 mm for optimal growth [14][21]. It also grows well in irrigated areas such as agricultural fields where rainfall is less than 500 mm [83][36]. It can withstand relatively dry climate conditions because of reserved water in the large roots, which was described in the Introduction [14,83][21][36].
This species grows well in the areas with a hot summer (over 25 °C) and mild winter (5–15 °C) [14][21]. The average mean temperature of the northern limit of this species was 7 °C in Japan (native range) [17][25]. The northward distribution of this species was thought to be limited by cold temperatures [70,85][15][40]. Its large leaves die back at the first frost in winter season, and regrow from the stem nodes in early spring [1][8]. The above-ground stems of this species survived at −26 °C in the North America [70,86][15][41]. This species also regrows from under-ground stems, and snow protects the under-ground stems from lethal temperatures [70,86][15][41]. In fact, P. montana has already infested Benzie County (northwest Michigan, USA), where a temperature of below −20 °C has been recorded 13 times in the past 30 years [87,88][42][43]. This species was also found in southern Ontario, Canada, where the coldest time of year recorded ranged from −26 °C to −29 °C [2,86][41][44].
A high degree of genetic diversity of the P. montana population in USA was found [76,89,90,91][22][45][46][47]. Its high genetic diversity may reflect the history of this species introduced into the USA. Multiple introductions occurred over a long time from different origins of the native ranges, and were followed by genetic exchanges among populations [1,76][8][22]. However, the genetic diversity of the species in the native ranges was within the average of that of the herbaceous perennial plant species [92,93][48][49]. Plant species with a high genetic diversity showed better potential for adaptation to various environmental conditions [94,95][50][51].

5. Allelopathy

The interaction of the alien plants with the indigenous plant species is one of the essential factors in the naturalization of alien plants in the introduced ranges [96,97,98,99][52][53][54][55]. Many invasive plants were reported to have an ability to perform allelopathy, which is the chemical interaction between donor plants and receiver plants [97,98,99,100][53][54][55][56]. Chemicals involved in allelopathy were defined as allelochemicals [100,101,102,103][56][57][58][59]. The allelochemicals are released into the neighboring environments including the rhizosphere soil from the donor plants through the rainfall leachates, volatilization, root exudation, and decomposition processes of donor plant residues. The allelochemicals are able to suppress the germination, growth and fitness of the neighboring plant species, and/or their mutualism with arbuscular mycorrhizal fungi and rhizobia [104,105,106,107,108][60][61][62][63][64]. Plants synthesize and store allelochemicals in some plant tissues until they release them into the neighboring environments [100,101,102,103][56][57][58][59]. Therefore, several researchers investigated the allelopathic activity in the extracts from different plant parts, the residues or litter of P. montana, and its rhizosphere soil.
Aqueous and methanol extracts of the leaves and roots of P. montana suppressed the germination and growth of Lactuca sativa L. and Raphanus sativa L., and the rhizosphere soil and litter of the species themselves suppressed the growth of Raphanus sativa and Lolium perenne L. Aqueous extracts of the litter of P. montana also suppressed the germination of Bidens pilosa L. and Lolium perenne. The pure soil mixed with the extracts of P. montana inhibited the root and shoot growth of Bidens pilosa and Lolium perenne. The total phenolic concentration in the P. montana-infested soil was 30- to 50-fold greater than that in the non-infested soil [109,110][65][66]. The investigations suggest that these phenolics may be involved in the inhibition caused by the litter and soils of P. montana. However, the chemical constituent of the phenolics has not been identified. The aqueous extracts of leaves, stems and roots of P. montana were also reported to suppress the germination of Taraxacum officinale F.H.Wigg, Lolium multiflorum Lam and Echinochloa crus-galli (L.) P.Beauv. [111][67].
The sterilized quart sand mixed with the leaf powder of P. montana inhibited the germination, and the root and shoot growth of Lepidium sativum L., Lactuca sativa, Phleum pratense L. Lolium multiflorum [112][68]. Two allelopathic active substances were then isolated form the leaves of P. montana, and identified as cis,trans-xanthoxin and trans,trans-xanthoxin. The concentration of cis,trans-xanthoxin and trans,trans-xanthoxin was 51 ng and 73 ng per g leaf fresh weight, respectively. cis,trans-Xanthoxin and trans,trans-xanthoxin inhibited the growth of Lepidium sativum at concentrations greater than 0.3 μM and 3 μM, respectively. The concentration required for causing a 50% growth inhibition was 1.1 μM and 14 μM for cis,trans-xanthoxin and trans,trans-xanthoxin, respectively [113][69]. cis,trans-Xanthoxin was converted to abscisic acid (plant hormone) in some plants and cell-free systems [114,115,116,117][70][71][72][73]. Although the concentration of trans,trans-xanthoxin in plants was always greater than that of cis,trans-xanthoxin [113[69][74],118], trans,trans-xanthoxin was not converted to abscisic acid [119][75]. Both cis,trans-xanthoxin and trans,trans-xanthoxin themselves showed growth inhibitory activity on several plant species [118[74][76],120], which indicates that both xanthoxins may function in some physiological processes in these plants. Therefore, cis,trans-xanthoxin and trans,trans-xanthoxin may also be involved in the allelopathy of P. montana.
When the protoplasts of P. montana and Lactuca sativa obtained from their cotyledons were incubated together, the growth of Lactuca sativa protoplasts was inhibited by P. montana protoplasts in a protoplast-concentration-dependent manner [121][77]. Daidzein, which is one of the major isoflavones in the leaves of P. montana [122[78][79],123], disturbed the cell wall formation and cell division of Lactuca sativa protoplasts [121][77]. Therefore, the protoplast cells of P. montana may secrete daidzein into the growth mediums, and the secreted daidzein inhibits the growth of Lactuca sativa protoplasts as an allelochemical. Daidzein was also reported to be active in several pharmacological aspects [124][80].
Phenylpropanoids such as p-coumaric acid, caffeic acid and methyl caffeate were identified in the roots of P. montana [125][81]. p-Coumaric acid and caffeic acid were found in several other plant species, and showed germination and growth inhibitory activity as allelopathic agents [126,127,128][82][83][84]. Caffeic acid suppressed the germination and growth of target plant species due to the disturbance of water transport and photosynthesis, and the induction of IAA-oxidation [129,130][85][86]. p-Coumaric acid also disturbed water transport, and reduced the contents of chlorophyll A and B, and photosynthesis [130,131][86][87].
These investigations suggest that leaves, roots and stems may contain water- and methanol-extractable allelochemicals, that some of them may be released from the residues or litter of this species into its rhizosphere soil, and that the soil may also contain some allelochemicals. cis,trans-Xanthoxin, trans,trans-xanthoxin, and daidzein were found in the leaves of P. montana, and may be involved in the allelopathy of P. montana. According to the novel weapons hypothesis, the competitive ability of invasive plants against indigenous plants is high due to the allelochemicals (weapons). These allelochemicals are released from the invasive plants, and enable the suppression of the germination, growth and regeneration of the indigenous plant species. These allelochemicals released from invasive plants are new to the indigenous plant species, because these indigenous plant species lack the co-evolutional history with the invasive plant species, and there has been no opportunity to develop tolerance towards these allelochemicals [96,97,133][52][53][88].

6. Insecticidal and Fungicidal Activity

The interaction between invasive plants and their natural enemies, such as herbivore insects and pathogens, is one of the important factors in the naturalization of invasive plants in the introduced ranges [98,134,135,136][54][89][90][91]. A moth species, soybean looper Pseudoplusia includens (Waker), was evaluated as a biocontrol agent for P. montana. However, the moths fed on P. montana showed a higher mortality and lower pupal weight than those fed on soybean [137][92], which suggests that certain compounds in the P. montana may be involved in the higher mortality and the lower pupal weight of the moths. The aqueous extract of P. montana suppressed the growth of the pathogenic fugus Colletotrichum lagenarium (Passerini) Ellis & Halsted, which was inoculated on the cotyledons and leaves of Cucumis sativus L. [138][93]. Two isoflavones, 7-acetyl-4′,6-dimethoxy-isoflavone and 7-acetyl-4′-hydroxy-6-methoxy-isoflavone, were isolated from P. montana and showed anti-tobacco mosaic virus activity [139][94]. These observations suggest that some compounds, including these isoflavones in P. montana, may work for anti-virus activity, and contribute to the fitness of P. montana into the introduced ranges.
Endophytes are present on the inside of plant tissues, and are involved in diverse and indispensable functions in plant growth, development, stress tolerance, and adaptation [140,141][95][96]. The interaction between endophytes and plants is species-specific, and most fungal endophyte species of P. montana belong to Ascomycota, Dothidemyceyes, Teremellales and Mycosphaerellaceae [142][97]. Some fungal endophytes in P. montana are involved in the growth suppression of pathogenic fungi such as Fusarium oxysporum [143][98]. Suppression was considered to be caused by the secretion of some secondary metabolites from the endophytes. These secondary metabolites suppressed the growth of the fungi as mycotoxins [144,145,146][99][100][101].
These investigations suggest that P. montana has anti-insecticidal and anti-virus activity and certain compounds, including isoflavones, may be involved in the activity. Endophytes in this species also suppress the growth of pathogenic fungi through mycotoxins. A great number of natural enemies such as herbivore insects and pathogens have been identified in P. montana stands in the native ranges in Japan and China [82,147,148][35][102][103]. However, fewer herbivore insects were found in the introduced ranges [11,22,149,150][32][33][104][105]. The condition of the existence of a few natural enemies may contribute to the superior growth rate and naturalization of P. montana in the introduced ranges.

7. Secondary Metabolites

P. montana is one of the most popular medicinal plants in Eastern Asia, and the dry roots and flowers of this species have been used in treatments of diabetes, fever, emesis, cardiac dysfunction and toxicosis [151,152,153][106][107][108]. Pharmacological investigations showed that the roots and flowers of P. montana contain a hundred polyphenolic compounds such as isoflavones, isoflavonoid glycosides, and saponins [154][109]. Isoflavones and their glycosides are the major pharmacological active constituents of these polyphenolic compounds, and puerarin and daidzein, among isoflavones and their glycosides, have been extensively investigated [155,156][110][111]. Puerarin is the most abundant secondary metabolite in the roots of P. montana, and showed a wide spectrum of pharmacological properties such as anti-diabetic activity, anti-inflammatory activity, anti-Parkinson’s disease activity, anti-Alzheimer’s disease activity, anti-isosteoporotic activity, and anti-cancer activity [155][110]. Daidzein was originally found in soybeans, and showed anti-diabetic activity and anti-inflammatory activity [157][112]. Alkaloids such as sophoridine and trigonelline were also found in the roots of P. montana [125][81]. Sophoridine showed anti-cancer, anti-inflammatory, and anti-bacterial activity [158][113]. Trigonelline was reported to show anti-Alzheimer’s disease activity and anti-diabetic activity [159][114].
Although the majority of the identified secondary metabolites in P. montana have not yet been connected to the invasiveness of the plant species, some of these compounds may be involved in the allelopathy and defense functions against herbivores and pathogens. In fact, the extracts of the roots, leaves and rhizosphere soil of P. montana showed inhibitory activity on the germination and growth of several plant species and insecticidal activity, as described in the above section. Plants contain a large number of secondary metabolites in several chemical classes. The biosynthesis of certain secondary metabolites is increased or synthesized de novo under specific conditions [100,160,161,162,163,164][56][115][116][117][118][119].

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