*Department of Botany, MES Abasaheb Garware College, Pune 4, MS, India

¹Department of Botany, Modern College of Arts, Science and Commerce, Pune 5, MS, India

Corresponding author email: gnivedita_ghayal@rediffmail.com

Article Publishing History

INTRODUCTION

The alien species highly out-compete the native species or escape from adverse environmental conditions and dominate the community (MacDougall and Turkington 2005).Their diversity is controlled by population, ecosystem dynamics, disturbances, nutrient supply and climatic factors. The biotic restrictions also force them to skip from their previous habitat and start surviving in new habitats, helping in the process of invasion (Mack et al. 2000). Many a times these phyto-invasives become very aggressive due to production of some defensive chemicals (Carpenter and Cappuccino 2005). These invasions pose many ecological, economic and social problems. Because of this the studies on plant invasions and its mechanism and consequences of them on global biodiversity and ecosystem functioning are of urgent need. This is because slowly and gradually these invasives become aggressive and encroach cultivable lands and pose a great problem (Chauhan et al. 2017).

Cassia uniflora Mill. non Spreng. (family- Caesalpinaceae) is annual, erect herb with yellow flowers and clustered pods. It originated in tropical South America and now distributed worldwide.  This invasive weed grows luxuriantly at many places (Almeida, 2003).  Synedrella nodiflora (L.) Gaertn. (family- Asteraceae) originated in tropical America, is an annual, erect, dichotomously branched herb distributed all over India (Almeida, 2003). Their dominance is attributed to wide adaptability to diverse habitat, different morpho-physiological characters and defensive allelo-chemicals (Ghayal et al.2007a,b; 2009; 2013).

Limited research has been done on the allelopathic effect or phyto-toxicity of Cassia uniflora to other plants. There is a general temper of agreement now-a-days that invasive plants displace the local biodiversity through their harmful effects including allelopathy (Cronk and Fuller, 1995). Allelopathic effects may due to the presence of allelochemicals in Cassia and Synedrella, like different types of phenolic compounds, alkaloids, triterpenoides, essential oils and flavonoids, biocides, juvenile hormones, growth hormones. They may be interacting with various physiological processes (Chatterjee et. al. 2012). From current literature review, it revealed that little research has been done on distribution, evolutionary studies and impact of Cassia uniflora and Synedrella nodiflora  on co-occuring species by using various tools of bioinformatics. The work done till now on the metabolic compounds and various allelochemicals has been restricted only to the wet lab methods and very little is known about the gene level expression of all such compounds. Some advanced researches show the gene expression analysis on different weeds that indicate several compounds responsible for the invasion of weeds into new environments ( Chen, 2013).

For bioinformatics study, several soft-wares and tools were used to analyse the data present on both the weeds. Due to lack of research on the weed plants, it was difficult to retrieve the molecular data. Hence the common enzymes in Cassia uniflora Mill. non Spreng, and Synedrella nodiflora (L) Gaertn, were selected for further analysis. The enzymes or proteins that were studied in both the invasive weeds are –  Maturase K [EC 2.7.10.2] and  Ribulose-1,5-bisphosphate carboxylase / oxygenase(Rubisco/ rbcL)[EC 4.1.1.39]. Maturase K is a plant plastidial gene. The protein it encodes is an intron Maturase, a protein that splices introns. Mat-K is proposed as the only chloroplast-encoded group II intron Maturase, thus implicating Mat-K in chloroplast posttranscriptional processing. For a protein-coding gene, mat-K has an unusual evolutionary significance, including relatively high substitution rates at both the nucleotide and amino acids levels, (Barthet et. al.2015).

The other enzyme that has been studied in both plants was ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) is the major enzyme assimilating CO₂ into the biosphere. At the same time Rubisco is an extremely inefficient catalyst and its carboxylase activity is compromised by an opposing oxygenase activity involving atmospheric O₂. These enzymes were considered for checking the probable similarity in the protein sequences of these two weeds. The nucleotide research on these enzymes is done intensively since both the enzymes play crucial role in plant metabolism. The focus of the study was to acquire the common factor based on genomic data in both the weeds that is responsible for their dominance and to understand and interpret their ecological and evolutionary significance.

The present work was carried out for correlating different genes or proteins in Cassia uniflora Mill. non Spreng and Synedrella nodiflora (L) Gaertn. responsible for their invasiveness by using different bioinformatics tools. Scanty information is available on the molecular level work, gene identification and sequencing of the invasive weeds as compared to the crop plants. Therefore present attempt was made to fulfil this gap in above mentioned weeds. It has also helped to get the idea about the ecological corridor developed by current dominant invasive weeds. Not only that but it has also helped to predict the future changes in weed flora and their ecological status.

MATERIAL AND METHODS

1. A) By performing Multiple Sequence Alignment (MSA):The Multiple Sequence Alignment of the 2 or more sequences was done to check whether the sequences align exactly similar to each other. Here, sequence homology is applied to assess if the sequences are sharing evolutionary origins. B) By using ‘Deep-view software’: This software was used for direct analysis of the similar or distant proteins. The proteins were modelled from the server ‘SWISSMODEL’ in PDB format to get the 3D structure. And then these proteins were analysed in the software. C) Preparation of phylogenetic tree: It was carried out to check the homology between the selected protein sequences. Cladistics analysis was performed by using software MEGA-X with the help of maximum likelihood method. Website used – ncbi.nlm.nih.gov

RESULTS AND DISCUSSION

For tracking down the upshots on invasive species Cassia uniflora/ Senna uniflora and Synedrella nodiflora the efforts were carried out in the following manner –A) By performing Multiple Sequence Alignment (MSA) – For Maturase-K and Rubisco for Cassia uniflora/ Senna uniflora and Synedrella nodiflora. B) By using ‘Deep-view software’- For protein structure of Maturase-K and Rubisco of Cassia uniflora/ Senna uniflora and Synedrella nodiflora. C) Preparation of phylogenetic tree / Cladistic analyses

C) Preparation of phylogenetic tree / Cladistic analyses –

Table 1. Phylogenetic trees of invasive species Cassia and Synedrella

No.	Type of Phylogenetic tree	Enzyme	MSA %
1.	Tree and herb species of Cassia/ Senna	Maturase-K	90%
2.	Tree and herb species of Cassia/ Senna	Rubisco	Negligible – the authenticity of this clad was very low and hence was not considered for comparison
3.	Weed species of Cassia/ Senna	Maturase-K	95%
4.	Weed species of Cassia/ Senna	Rubisco	90%
5.	Synedrella nodiflora and other weed species	Maturase-K	60%
6.	Synedrella nodiflora and other weed species	Rubisco	90%
7.	Cassia/ Senna, Synedrella and other related genera and species	Maturase-K	80%
8.	Cassia/ Senna, Synedrella and other related genera and species	Rubisco	85-90%

1. A) Results of Multiple Sequence Alignment (MSA):Multiple sequence alignment showed that the sequence of enzyme ‘Maturase-K’ is exactly similar in plants Cassia unifloraand Synedrellanodiflora. This result revealed the sequences with almost homologous regions showing ‘*’symbol as exactly matching sequences (Fig.1, Table 2). Similar MSA was carried out on Rubisco for the same two plants Cassia uniflora and Synedrella nodiflora and equivalent similarity was observed. The figure and table for this are not included to avoid repetition of the sets.

A) By Multiple Sequence Alignment (MSA)

MSA of Cassia uniflora and Synedrella nodiflora for Maturase-K enzyme-

Figure 1: Showing Multiple Sequence Alignment for Maturase-K enzyme

Table 2. Showing details of two weeds used for MSA of Maturase-K enzyme

Name of the Plant	Accession Number	Number of Base Pairs (Amino acids)	Included or Excluded	MSA percentage of Sequence Similarity All these species show about 70 % sequence similarity
Cassia uniflora	ARR68700.1	280	Included
Synedrella nodiflora	AAR02837.1	508	Included

When similar MSA (Multiple sequence alignment/s) was carried out for Rubisco enzyme,   Cassia  auriculata had to beexcepted because it has different base pairs than all other plants which was affecting the comparison among the selected plants. The comparison of remaining plants showed almost similar sequences in all the species related to the weed species under consideration i.e. Cassia uniflora and Synedrella (Fig. 2, Table 3). Similar comparison is done for Maturase-K enzyme and it shows similar results except the inclusion of Cassia auriculata. Hence it can be predicted that these invasive species could have evolved in similar way for the enzymes like ‘Maturase-K’ and Rubisco.

MSA for all related species of both Cassia uniflora and Synedrella nodiflora for Rubisco enzyme –

Figure 2: Showing Multiple Sequence Alignment for Rubisco

Table 3: Showing details of nine plants used for MSA of Rubisco enzyme

Name of the Plant	Accession Number	Number of Base Pairs (Amino acids)	Included or Excluded	MSA percentage of Sequence Similarity
Cassia uniflora	AQY09936.1	249	Included	All these species together show about 80 % sequence similarity
Cassia obtusifolia	ADD48483.1	234	Included
Cassia tora	AYF60003.1	238	Included
Cassia auriculata	AII33731.1	290	Excluded
Cassia occidentalis	AZC11295.1	416	Included
Cassia sophera	AFU54416.1	202	Included
Synedrella nodiflora	ARR11741.1	468	Included
Tridax procumbens	AFP23718.1	461	Included
Pulicaria dysenterica	AKG25301.1	439	Included

Results of using ‘Deep-View’ software: When the models of protein structures for both the enzymes ‘Maturase-K’ and ‘Rubisco’ were run in Deep view software, models exhibited similar sequences of both the enzymes that implied the similar structures and hence all the models tracked in the software were able to get merged. Results of deep view analysis (Fig. 3 & 4) showed that the enzymes studied had identical structures and the highlighted portion in both the images showed shared structures of the same protein but in two different plants Cassia / Senna  unifloraand Synedrella. This probable further confirms simultaneous evolution of these invasive species and their imperative enzymes.

Figure 3: Circled portion indicates common sequence coding similar structure of enzyme MATURSE-K in Cassia uniflora and Synedrella nodiflora

Figure 4: Circled portion indicates common sequence coding similar structure of enzyme RUBISCO in Cassia uniflora and Synedrella nodiflora

Preparation of phylogenetic trees / Cladistic analyses: The construction of phylogenetic trees was carried out with the interest of searching the evolutionary associations of Cassia/ Senna uniflorawith the other native, weedy and less dominant species of Cassia.  In case of Synedrella searching was attempted with the same approach but due to very much insubstantial outcomes, the cladograms were developed based on few weedy, local and fairly prevailing genera and species from the same family Asteraceae, as this family is well known to contain globally distributed, highly dominant invasive weed genera other than Synedrella.

The Cladistic analysis (Fig. 5, Table 4) performed on different herb and tree species of Cassia revealed that Cassia uniflora had a distant phylogeny and did not share any recent ancestry with any of the other Cassia species for Maturase-K enzyme.As against that when the phylogenetic comparison of different weed species of Cassia / Senna was carried out for these two enzymes, it was observed that Cassia unifloraand Cassia auriculatamight have progressed in the most parallel way and from very recent common ancestor in due course of evolution (Figures 6, 7; Tables 5,6). It can also be confirmed by the habitat of both the species of Cassia. Both Cassia uniflora and Cassia auriculata grow intensively in semi-arid conditions. The similar phylogeny here, in both the enzymes, Maturase-K and Rubisco, suggests that these two plants must have acquired similar properties that help them survive under the unfavourable conditions and this could be the key to their dominance over other native plants. The results showed that the evolution of Cassia uniflora and Cassia auriculata is relatively similar to each other over other species of Cassia. Cassia uniflora  is the most dominant species of the genus Cassia presently and Cassia auriculata might evolve further as dominant species in subsequent situations of environment, as Cassia uniflora is today. The other species of Cassia such as Cassia occidentalis and Cassia tora have shown distant phylogeny. Both Cassia uniflora and Cassia auriculata are distantly evolved from other species of Cassia and hence show significantly different habitat and possibly also the chemical properties than other members of genus Cassia.

1. Preparation of phylogenetic tree / Cladistic analyses

Cladistics analysis between different species ofCassia for Maturase-K enzyme-

Figure 5: Comparison between different species of Cassia for maturase-K enzyme

Table 4. Showing details of different species of Cassia for Maturase-K enzyme

Name of the Plant	Accession Number	Number of Base Pairs (Amino acids)	Included or Excluded	MSA percentage of Sequence Similarity All these species show about 90 % sequence similarity
Cassia uniflora	ARR68700.1	280	Included
Cassia roxburghii	AFU54442.1	278	Included
Cassia javanica	AFU54432.1	278	Included
Cassia leptophylla	APZ80402.1	499	Included
Cassia javanica var. indochinensis	AFC38374.1	501	Included
Cassia fistula	ARO84601.1	501	Included

Cladistics analysis between weed species of Cassia for Maturase-K enzyme–

Figure 6: Showing Phylogenetic tree of four weed species for Maturase-K enzyme

Table 5. Showing details of four weed species of Cassia used for MSA of Maturase-K enzyme

Name of the Plant	Accession Number	Number of Base Pairs (Amino acids)	Included or Excluded	MSA percentage of Sequence Similarity All these species show about 95 % sequence similarity
Cassia uniflora	ARR68700.1	280	Included
Cassia obtusifolia	ASU41854.1	276	Included
Cassia tora	AJM88385.1	248	Included
Table 5: Showing details of four weed species of Cassia used for MSA of Maturase-K enzyme Cassia auriculata	ARR68699.1	261	Included

The comparison of Synedrella in cladogram with the other genera of asteraceae for Maturase-K showed that, number of base pairs varies greatly among genera and hence the MSA percentage has fallen (60%) but the matching base pairs show completely identical sequences for all the plants. Synedrella nodiflora indicated distant phylogeny from Tridax procumbens and Pulicaria dysenterica but is relatively nearer to Lactuca indica (Fig. 8, Table 7). These three genera of Asteraceae show their frequent but less dominant occurrence than Synedrella.For the same members of asteraceae, the building up of phylogenetic tree for Rubisco was performed excluding Lactuca indica as its protein sequence was unavailable. Here, it was observed that Tridax procumbens and Pulicaria dysenterica had the closest phylogeny showing Synedrella nodiflora distantly placed (Fig. 9, Table 8).

Figure 7: Showing phylogenetic tree of weedspecies for Rubisco enzyme

Table 6. Showing details of weedspecies for Rubisco enzyme

Name of the Plant	Accession Number	Number of Base Pairs (Amino acids)	Included or Excluded	MSA percentage of Sequence Similarity All these species show about 90 % sequence similarity
Cassia uniflora	AQY09936.1	249	Included
Cassia obtusifolia	ADD48483.1	234	Included
Cassia tora	AYF60003.1	238	Included
Table 6: Showing details of weedspecies for Rubisco enzyme Cassia auriculata	AII33731.1	290	Excluded

Cladistics analysis for Synedrella nodiflora withherb species of Asteraceae family members for Maturase-K enzyme

Figure 8: Showing Phylogenetic tree of herb species of members of Asteraceae for Maturase-K enzyme

Table 7. Showing details of asteraceae members herb species for Maturase-K enzyme

Name of the Plant	Accession Number	Number of Base Pairs (Amino acids)	Included or Excluded	MSA percentage of Sequence Similarity All these species show about 60 % sequence similarity
Synedrella nodiflora	AAR02837.1	506	Included
Tridax procumbens	AZC11634.1	254	Included
Lactuca indica	ACY71114.1	506	Included
Table 7: Showing details of asteraceae members herb species for Maturase-K enzyme Pulicaria dysenterica	AFC83880.1	324	Included

The comparison of both Cassia uniflora and Synedrella  nodiflora for Maturase-K showed very distant origin. Cassia uniflora showed quite distant phylogeny from other Cassia species (Fig. 10, Table 9) whereas; Synedrella nodiflora shares similar phylogeny with Lactuca indica. In contrast the comparison for Rubisco showed common ancestry for Cassia uniflora and Synedrella nodiflora as they are placed very close to each other (Fig. 11, Table 10). This shows that both the plants might have developed different evolutionary patterns than all the other plants under consideration which resulted in distant phylogeny of both. In this clad, Lactuca indica was not considered for the comparison as its protein sequence for Rubisco was unavailable (Fig. 11, Table 10). The importance of genomic tactics for understanding the weedy and invasive behaviours of plants, their evolution and resistant response to environmental fluctuations is better realised now as a part of weed biology ( Stewart et al. 2009).

Cladistics analysis for Synedrellanodiflorawith herb species of Asteraceae family members for Rubisco enzyme –

Figure 9: Showing Phylogenetic tree of herb species of members of Asteraceae for Rubisco enzyme

Table 8: Showing details of herb species of members of Asteraceae for Rubisco enzyme

Table 8. Showing details of herb species of members of Asteraceae for Rubisco enzyme

Name of the Plant	Accession Number	Number of Base Pairs (Amino acids)	Included or Excluded	MSA percentage of Sequence Similarity All these species show about 90 % sequence similarity
Synedrella nodiflora	AAR11741.1	468	Included
Tridax procumbens	AFP23718.1	461	Included
Lactuca indica	–	–	Excluded
Table 8: Showing details of herb species of members of Asteraceae for Rubisco enzyme Pulicaria dysenterica	AKG25301.1	439	Included

Cladistics analysis for weed related species of both Cassia uniflora and Synedrella nodiflora for Maturase-K enzyme –

Figure 10: Showing Phylogenetic tree of all 9 species for Maturase-K enzyme

Table 9. Showing details of weedspecies for Maturase-K enzyme

Name of the Plant	Accession Number	Number of Base Pairs (Amino acids)	Included or Excluded	MSA percentage of Sequence Similarity All these species together show about 80 % sequence similarity
Cassia uniflora	ARR68700.1	280	Included
Cassia obtusifolia	ASU41854.1	276	Included
Cassia tora	AJM88385.1	248	Included
Cassia auriculata	ARR68699.1	261	Included
Cassia occidentalis	AZC11603.1	269	Included
Cassia sophera	AFU54436.1	278	Included
Synedrella nodiflora	AAR02837.1	506	Included
Tridax procumbens	AZC11634.1	254	Included
Lactuca indica	ACY71114.1	506	Included
Table 9: Showing details of weedspecies for Maturase-K enzyme Pulicaria dysenterica	AFC83880.1	324	Included

It further opens a new research route for perception of reckless growth and evolution of phyto-invasives and their functioning under harsh stress conditions. It also shares knowledge about weed management, herbicide resistance mechanism of allelopathy and evolution of invasiveness of such plant species (Thomas and Klaper, 2004).  Such phylogenetic studies using various methods help to better understand causes of invasion success, ecosystem disturbance and alterations in biodiversity (Forest et al., 2007; Proches et al., 2008; Winter et al., 2009; Dawson et al., 2009).

Cladistics analysis for weed related species of both Cassia uniflora and Synedrella nodiflora for Rubisco enzyme –

Figure 11: Showing Phylogenetic tree of all 9 species for Rubisco enzyme

Table 10. Showing details of weed species for Rubisco enzyme

Name of the Plant	Accession Number	Number of Base Pairs (Amino acids)	Included or Excluded	MSA percentage of Sequence Similarity All these species together show about 90 % sequence similarity
Cassia uniflora	AQY09936.1	249	Included
Cassia obtusifolia	ADD48483.1	234	Included
Cassia tora	AYF60003.1	238	Included
Cassia auriculata	AII33731.1	290	Included
Cassia occidentalis	AZC11295.1	416	Included
Cassia sophera	AFU54416.1	202	Included
Synedrella nodiflora	AAR11741.1	468	Included
Tridax procumbens	AFP23718.1	461	Included
Lactuca indica	–	–	Excluded
Table 10: Showing details of weed species for Rubisco enzyme Pulicaria dysenterica	AKG25301.1	439	Included

Some studies have also claimed that phylogenetic and functional attributes of alien species readdress different aspects of ecosystem functioning and variations produced at the level of organisms (Chen, 2013; Ricotta et al. 2009, 2010; Cadotte et al. 2009). According to some researchers unusual characters and ancestral relations with natives probably are promoting the aliens to become invasive very swiftly in non-native ranges of global vegetation (Clements and Ditommaso, 2011).Bezeng et al. (2013) have claimed that phylo-genomic studies of invasive species with reference to their native co-survivors are the most important drivers of ecosystem change, which can alter the vegetational set up of a particular area. Similar studies on Maturase-K and Rubisco of island flora have been carried out by them to understand the causes of invasion on Robben island, South Africa. The results recorded in the figures 1 and 2 and Tables 2 and 3 showed that multiple sequence alignments are shared for Maturase-K and Rubisco of Cassia uniflora and Synedrella. Deep view analysis (Figures 3 and 4) also revealed major portions identical for both the enzyme proteins for C. uniflora and Synedrella. This further indicates that these two enzymes might be the drivers in the invasion success of C. uniflora and Synedrella(Bezeng et al., 2013), since these enzymes have prime importance in the plant metabolism.

When evaluation of different species of Cassia for Maturase-K was carried out (Fig. 5, Table 4), it exhibited minor likelihood of C. uniflora from others. Further, when we examined the cladistics patterns of different species of Cassia for both the enzymes (Figures  6, 7  and Tables 5, 6), it was observed that C. auriculata is lineally related to C. uniflora, indicating similar or parallel functional traits which are essential for invasion. Martyniuk et al. (2009) have phyletically compared members of Amaranthaceae in the same way for pollen structures based on these two enzymes.The evaluation of different asteraceae members along with the invasive alien species Synedrellanodiflorasuggested its racial link with Lactucaindica for Maturase-K (Fig.8, Table 7). When Synedrellanodiflorawas (Fig. 9, Table 8) compared with same herb species from asteraceae for Rubisco revealed distant phylogeny. The consideration for phyletic relatedness when was performed for Maturase-K (Fig. 10, Table 9), showed totally separate placement of C. uniflora but indicating probable common ancestry. This clad suggested co-evolution of  Synedrella nodiflora and Lactuca indica. The same set of plants was used to prepare clad for Rubisco revealed (Fig. 11, Table 10) the diversification from the common inherited line. The studies on evolutionary population genomics in the Asteraceae family have been carried out by Stevens (2007), Barker et al. (2008), Broz et al. (2007) and  Mandel et al. (2017).

Thus the present study has facilitated to establish the correlations of the invasive species Cassia uniflora and Synedrella nodiflora with the other innate and aggressive species either of the same genus or family. The phylogenomic studies using bio-computing tools enabled to understand the protein nature of Maturase-K and Rubisco of these two weeds mainly and also of other species. There could be generated various clades giving insights into the evolutionary connections of these aliens developing monothickets with each other along with the other plants. Further it will help to know the changing and dominating weed flora in the same area.

CONCLUSION

Overall this research work points out to the protein based phylogenetic similarities and distinctiveness of alien taxa with respect to the other genera as significant details deciding their invasion success (Ordonez, 2014). This enhances to the idea of phylogenetic and metabolic patterns of successfully invaded species. Further these studies have focussed light on the future invasive followers of them on Deccan plateau through different probability patterns.

ACKNOWLEDGEMENTS

The authors are thankful to Principal and Head, Department of Botany, MES Abasaheb Garware College, Pune and Modern College of Arts, Science and Commerce, Shivajinagar, Pune, for their constant support in carrying out this research.

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