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Molecular Adaptation of rbcL in the Heterophyllous Aquatic Plant Potamogeton

Heterophyllous taxa usually produce floating or terrestrial leaves in the summer [3] , [35]. To improve their intrinsic thermal stability, proteins have more hydrophobic residues with branched side chains and more charged residues, at the expense of uncharged polar residues [37]. Molecular evolutionary analysis of cyanobacteria RbcL suggests that adaptive replacement, an increase in hydrophobic residues and a decrease in uncharged polar residues, occurred in a clade of hot spring strains [20].

In Potamogeton RbcL, the uncharged polar residue Ser was replaced with the hydrophobic residue Ala at site Table 3. This amino acid replacement might increase the thermal stability of RbcL in the heterophyllous taxa. However, recent evolutionary analyses of RuBisCO suggested that amino acid site underwent parallel genetic changes; the Ala in almost all C 3 photosynthesis species was replaced by Ser in the C 4 group [23]. The replacement of Ala by Ser occurred in two homophyllous species P.

The detection of positive selection in heterophyllous lineages suggested that selective pressure on this chloroplast gene was higher for heterophyllous lineages than for homophyllous lineages.

Plant Adaptation to Changing Environment

In the evolutionary analyses of rbcL sequences from over species representing green plants and other phototroph lineages, the neighboring residues and in helix 4 were identified as evolving under positive selection [22]. This suggests that a replacement at these amino acid sites could be involved in the adaptation of specificity or catalytic efficiency to widespread environmental variation in temperature and dryness in both terrestrial land plants C 4 and C 3 plants and Potamogeton.

Many aquatic plants have acquired carbon-concentrating mechanisms to overcome the potentially low, fluctuating supply of CO 2 for underwater photosynthesis [38]. A strategy of C 4 -like carbon fixation operates in several freshwater homophyllous species [38] — [40] and seagrasses [41]. The evolutionary analysis of the RuBisCO gene revealed that five amino acid sites in rbcL evolved under positive selection in terrestrial C 4 monocots [23].

At three amino acid sites, residues of the C 4 -like seagrass Zostera were fixed and shared with those of terrestrial C 4 monocots Ile , Ile , and Ser [42].

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The homophyllous species P. This plant tends to be shade tolerant and grows in deep fresh water and brackish water [11].

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Its sister species P. Our ongoing studies indicate that underwater heat stress induces the transcription of key enzymes in C 4 photosynthesis phosphoenolpyruvate carboxylase and pyruvate, orthophosphate dikinase in submerged leaves of P. This suggests that amino acid replacement in P. However, the selective pressure involved appeared to be mild, as no positive selection specific to homophyllous lineages was detected. Our analysis did not show an exact relationship between the amino acid replacements and heterophylly or homophylly but revealed that positive selection has affected the Potamogeton rbcL.

Polyploidy and aneuploidy, major forces in diversification, are common within the genus [43]. We are now conducting phylogenetic analyses of four nuclear genes to infer the polyploid history of Japanese Potamogeton. Our preliminary data suggest that heterophylly has evolved through allopolyploid formation.


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The increased amino acid replacement in rbcL may reflect the adaptive fine-tuning of RuBisCO in the alternation of growth forms heterophyllous or homophyllous and nuclear genome setsz. Japanese Potamogeton species and the allied species Stuckenia pectinata L. We categorized the Potamogeton species into three groups based on growth form and leaf type: homophyllous species submerged leaves , floating-leaved heterophyllous species submerged and floating leaves , and terrestrial-leaved heterophyllous species submerged, floating, and terrestrial leaves , according to the descriptions of Kadono [44].

The production of terrestrial leaves has been observed in some homophyllous species P. Nevertheless these species were treated as homophyllous, as their terrestrial leaves did not seem to contribute to persistent survival. The amplification and sequence analysis of chloroplast-encoded genes rbcL , atpB , and petA were performed as described previously [9]. The forward and reverse primers used for amplification are listed in Table S2. Five starting trees neighbor-joining and four equally parsimonious trees were examined with the substitution model HKY85, and the phylogenetic tree with the largest likelihood was selected.

Stuckenia pectinata was used as the outgroup. Two length mutations a 9-bp deletion in P. Molecular adaptation tests on the Potamogeton rbcL codon sites and reconstruction of the ancestral rbcL sequences were performed using maximum-likelihood models and programs included in PAML ver. We used five site-specific codon substitution models: null models for testing positive selection M1A, M7, and M8A and models allowing for positive selection M2A and M8 [50] , [51]. The likelihood ratio test was used to compare these alternative models. To clarify whether positive selection is linked to the evolution of heterophylly or homophylly, the branch-site models implemented in PAML ver.

As a single origin of heterophylly is more parsimonious than multiple origins, subgroup Ia was assigned as a heterophyllous lineage for the selection test, in addition to the other monophyletic lineages of heterophyllous species Fig. Such a definition of heterophyllous lineage was considered logical, as the homophyllous species included in subgroup Ia P.

A site was considered potentially under positive selection when it had probabilities above 0. All the above molecular evolutionary analyses were also carried out for the other chloroplast genes, atpB and petA. To identify the amino acid position for the structural motif, the quaternary structure of RbcL was inferred from data for Spinacia oleracea L. List of Potamogeton and Stuckenia species with GenBank accession numbers of chloroplast genes examined in the present study. Parameter estimates and log-likelihood values for Potamogeton atpB under eight codon substitution models included in PAML.

Parameter estimates and log-likelihood values for Potamogeton petA under eight codon substitution models included in PAML. LRT statistics for testing the hypothesis of positive selection in Potamogeton chloroplast genes. We thank Dr. Performed the experiments: SI AM. Analyzed the data: SI SA. Wrote the paper: SI KK. Browse Subject Areas? Click through the PLOS taxonomy to find articles in your field. Abstract Background Heterophyllous aquatic plants show marked phenotypic plasticity.

Principal Findings Phylogenetic and maximum likelihood analyses of codon substitution models indicated that Potamogeton rbcL has evolved under positive Darwinian selection. Funding: The authors have no support or funding to report. Introduction Many aquatic plants exhibit marked developmental plasticity, known as heterophylly. Download: PPT. Figure 1. Table 1.

Parameter estimates and log-likelihood values for Potamogeton rbcL under eight codon substitution models included in PAML. Table 2. LRT statistics for testing the hypothesis of positive selection in Potamogeton rbcL. Features of amino acid replacement sites Table 3 shows the distribution of 12 variable amino acid sites in RbcLs from Potamogeton and the outgroup species. Table 3. Amino acid replacement sites in 18 Potamogeton species and Stuckenia RbcL. Discussion In Potamogeton , heterophyllous species are distributed in freshwater and sometimes on the shore, whereas homophyllous species live entirely underwater in fresh or brackish water.

Conclusion Our analysis did not show an exact relationship between the amino acid replacements and heterophylly or homophylly but revealed that positive selection has affected the Potamogeton rbcL. Amplification and sequencing of chloroplast-encoded genes The amplification and sequence analysis of chloroplast-encoded genes rbcL , atpB , and petA were performed as described previously [9].

Supporting Information. Table S1. Table S2. List of primers used for PCR. Table S3. Table S4. Table S5. Text S1. Abstract in Japanese. Additionally, world's resources of P are limited Vance et al, Unlike nitrate, which readily moves in soil towards the roots via both mass flow and diffusion, phosphate ion is highly immobile in mineral soils.

However, the diffusion coefficient for phosphate ion in soil is very low compared to those for other nutrients Clarkson, ; consequently, plants do not deplete the total volume of the rooted soil layer but only that part of the soil which is in the immediate vicinity of the roots Fohse and Jungk, Phosphorus is commonly bound to iron and aluminium oxides and hydroxides through chemical precipitation or physical adsorption Kochian et al.

The rest stays in the soil and may be used by crops in the following years. Because of low P solubility and desorption, only a small proportion of phosphate ions exist in the soil solution for plant uptake even under optimum P fertilization making P fertilizer recovery to be lower compared to other nutrient containing fertilizers Holford, This suggests that chemical fertilizer application alone is not a cost effective way of increasing crop production in many P-limiting soils Tilman et al.

Study Finds Genetic Clues to How Plants Adapt to Climate

Soil phosphorus management options for sustainable crop production. Sustainable crop production aims at maintaining high crop yield without adversely affecting ecosystems to meet the need of current as well as future generations Tilman et al. Since phosphorus in agriculture is the second most growth limiting macronutrient af ter nitrogen, its proper management in soil contributes significantly to sustainable crop production.


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In such soils where yield is limited because of inherent low P concentration P deficient soils , application of relatively higher amount of mineral P fertilizers is the only way to enhance soil available P status to a target value in a long run that can sustain high crop yield.