Rice Science ›› 2022, Vol. 29 ›› Issue (1): 31-46.DOI: 10.1016/j.rsci.2021.12.003
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Shalini Pulipati1, Suji Somasundaram1, Nitika Rana2, Kavitha Kumaresan3, Mohamed Shafi4, Peter Civáň5, Gothandapani Sellamuthu1,6, Deepa Jaganathan7, Prasanna Venkatesan Ramaravi8, S. Punitha1, Kalaimani Raju1, Shrikant S. Mantri2, R. Sowdhamini4, Ajay Parida9, Gayatri Venkataraman1()
Received:
2021-01-23
Accepted:
2021-05-17
Online:
2022-01-28
Published:
2022-01-01
Contact:
Gayatri Venkataraman
Shalini Pulipati, Suji Somasundaram, Nitika Rana, Kavitha Kumaresan, Mohamed Shafi, Peter Civáň, Gothandapani Sellamuthu, Deepa Jaganathan, Prasanna Venkatesan Ramaravi, S. Punitha, Kalaimani Raju, Shrikant S. Mantri, R. Sowdhamini, Ajay Parida, Gayatri Venkataraman. Diversity of Sodium Transporter HKT1;5 in Genus Oryza[J]. Rice Science, 2022, 29(1): 31-46.
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O. sativa (Negrão et al, | 1 | 2 | 3 | 4 | 5 | 6 | 7 | 8 | 9 | 10 | 11 | O. sativa (Platten et al, |
---|---|---|---|---|---|---|---|---|---|---|---|---|
S2N | S | S | S | S | S | S | S | S | S | S | S | JQ695816: N |
F66L | F | F | F | F | F | F | F | F | F | F | F | F |
T67K | T | T | T | T | T | T | T | T | T | T | T | T |
A123P | A | A | A | A | A | G | G | A | A | A | T | JQ695818: P |
D128N | D | D | D | D | D | - | - | H | H | - | H | JQ695815: N |
S134N | S | S | S | S | S | - | - | - | - | S | - | JQ695818: N |
*P140A | P | A | P | P | P | P | P | P | P | P | P | JQ695815, JQ695814, JQ695812, JQ695817: A |
P144R | P | P | P | R | R | T | T | T | T | P | L | P |
V162L | V | V | F | V | V | V | V | V | V | I | N | V |
*R184H | R | H | R | R | R | S | S | S | G | S | S | JQ695814, JQ695812, JQ695817: H |
S197P | S | S | S | S | S | - | - | - | - | - | - | JQ695818 |
L231V | L | L | L | L | L | L | L | L | L | L | L | L |
A233V | A | A | A | A | A | V | V | I | V | V | I | JQ695818 |
*H332D | H | D | D | D | D | D | D | D | D | D | D | JQ695814, JQ695812, JQ695817, JQ695816, JQ695818: D |
S338P | S | S | S | P | P | A | A | S | S | S | S | S |
V349M | V | V | V | V | V | V | V | V | V | V | V | V |
G364S | G | G | G | S | S | A | Y | Y | G | G | G | G |
*L395V | L | V | V | V | V | V | V | V | V | V | V | All V |
P508S | P | P | P | S | S | P | P | P | P | P | P | P |
L531F | L | L | L | L | L | L | L | L | L | L | L | L |
Q429K | Q | Q | K | Q | Q | Q | Q | Q | Q | Q | Q | JQ695818, JQ695816: K |
1, O. sativa ssp. japonica (AA); 2, O. sativa ssp. indica (AA); 3, O. nivara (AA); 4, O. glaberrima (AA); 5, O. barthii (AA); 6, O. punctate (BB); 7, O. minuta (BBCC); 8, O. officinalis (CC); 9, O. alta (CCDD); 10, O. brachyantha (FF); 11, O. coarctata (KKLL). Blue, green or yellow colours indicate conserved amino acid residues in related Oryza species. Corresponding amino acid residues in O. sativa HKT1;5 sequences (landraces/varieties) reported by Platten et al ( |
Table 1. Non-synonymous amino acid substitutions in O. sativa HKT1;5 sequences reported by Negrão et al (2013) and comparison with those from Oryza species.
O. sativa (Negrão et al, | 1 | 2 | 3 | 4 | 5 | 6 | 7 | 8 | 9 | 10 | 11 | O. sativa (Platten et al, |
---|---|---|---|---|---|---|---|---|---|---|---|---|
S2N | S | S | S | S | S | S | S | S | S | S | S | JQ695816: N |
F66L | F | F | F | F | F | F | F | F | F | F | F | F |
T67K | T | T | T | T | T | T | T | T | T | T | T | T |
A123P | A | A | A | A | A | G | G | A | A | A | T | JQ695818: P |
D128N | D | D | D | D | D | - | - | H | H | - | H | JQ695815: N |
S134N | S | S | S | S | S | - | - | - | - | S | - | JQ695818: N |
*P140A | P | A | P | P | P | P | P | P | P | P | P | JQ695815, JQ695814, JQ695812, JQ695817: A |
P144R | P | P | P | R | R | T | T | T | T | P | L | P |
V162L | V | V | F | V | V | V | V | V | V | I | N | V |
*R184H | R | H | R | R | R | S | S | S | G | S | S | JQ695814, JQ695812, JQ695817: H |
S197P | S | S | S | S | S | - | - | - | - | - | - | JQ695818 |
L231V | L | L | L | L | L | L | L | L | L | L | L | L |
A233V | A | A | A | A | A | V | V | I | V | V | I | JQ695818 |
*H332D | H | D | D | D | D | D | D | D | D | D | D | JQ695814, JQ695812, JQ695817, JQ695816, JQ695818: D |
S338P | S | S | S | P | P | A | A | S | S | S | S | S |
V349M | V | V | V | V | V | V | V | V | V | V | V | V |
G364S | G | G | G | S | S | A | Y | Y | G | G | G | G |
*L395V | L | V | V | V | V | V | V | V | V | V | V | All V |
P508S | P | P | P | S | S | P | P | P | P | P | P | P |
L531F | L | L | L | L | L | L | L | L | L | L | L | L |
Q429K | Q | Q | K | Q | Q | Q | Q | Q | Q | Q | Q | JQ695818, JQ695816: K |
1, O. sativa ssp. japonica (AA); 2, O. sativa ssp. indica (AA); 3, O. nivara (AA); 4, O. glaberrima (AA); 5, O. barthii (AA); 6, O. punctate (BB); 7, O. minuta (BBCC); 8, O. officinalis (CC); 9, O. alta (CCDD); 10, O. brachyantha (FF); 11, O. coarctata (KKLL). Blue, green or yellow colours indicate conserved amino acid residues in related Oryza species. Corresponding amino acid residues in O. sativa HKT1;5 sequences (landraces/varieties) reported by Platten et al ( |
Fig. 1. HKT1;5 expression in Oryza species in leaf and root tissues under control and salinity treated conditions (incremental salinity application). Data are Mean ± SE for two biological replicates (each biological replicate was analyzed by qRT-PCR twice, each time in triplicate). Gene expression was quantified using the comparative CT (2-ΔΔCT) quantitation method with values representing ‘n’-fold difference relative to the housekeeping control gene β-Actin. Significance was calculated using the Student’s t-test. **, P < 0.01, ***, P < 0.001 and ****, P < 0.0001.
Fig. 2. O. coarctata BAC clone Oc_Ba_0043B05 sequencing and annotation. A, Genomic alignment of O. coarctata Oc_Ba_0043B05 sequence with orthologous region of O. sativa (japonica) on chromosome 1. Predicted FGNESH gene models are indicated by pink boxes while retrotransposon gene models are indicated by grey boxes. Red arrows indicate gene orientation. Orthologous region in japonica is indicated by a green line. Gene models I?V are present. In addition, two gene insertions are also present in the japonica sequence that are absent in the assembled O. coarctata BAC sequence. B, Predicted exon/intron organizations of gene models (I?V) for O. coarctata Oc_Ba_0043B05 sequence are conserved in japonica rice. C, Predicted protein lengths of models I?V and accession numbers of corresponding japonica transcript orthologs. Asterisks indicate gene models validated in O. coarctata transcriptome or by qRT-PCR (unpublished).
Fig. 3. Alignment of O. coarctata HKT1;5 homoeologous genomic and protein sequences. A, Dot plots showing four aligned regions of O. coarctata Oc_Ba_0043B05 sequence (143 522 bp) and OcHKT1;5-L genome (2 746 bp) sequences. BAC clone coordinates corresponding to four regions of homology (encompassing OcHKT1;5-K) with OcHKT1;5-L are indicated: (i) 115 810 to 117 107 (88% identity), (ii) 112 615 to 113 365 (87% identity), (iii) 115 067 to 115 333 (84% identity), and (iv) 113 686 to 114 009 (81% identity). B, Alignment of OcHKT1;5-K (521 amino acid residues) and OcHKT1;5-L (535 amino acid residues) translated open reading fragments. The selectivity filter residues ‘S-G-G-G’ are marked by red asterisks while the selectivity filters are boxed in red. Conserved amino acid residues near the ion pore entrance crucial to ion transport are marked by a red dot. Amino acid residues indicated by red, green, dark blue or purple dots occur near the ion pore entrance and are the same in OcHKT1;5-K and OcHKT1;5-L. Resides marked by pink and light blue dots near the ion pore entrance show opposite charges in OcHKT1;5-K and OcHKT1;5-L. Pink asterisks indicate residues that are part of an extracellular putative cation coordination site. Black asterisks indicate residues that differ between OcHKT1;5-K and OcHKT1;5-L and either occur in transmembrane segments or in loops oriented towards the ion pore entrance.
Fig. 4. Homology models and electrostatic maps of OcHKT1;5-K and OcHKT1;5-L proteins. A and B, Model monomers of OcHKT1;5-K (A) and OcHKT1;5-L (B). Key residues at the pore entrance are highlighted as spheres, and the length between residues has been measured. Extracellular cation coordination sites (magenta) and residue differences within 2 nm from the pore region of both model (blue) are highlighted. C and D, Comparative electrostatic maps of model generated for OcHKT1;5-K (C) and OcHKT1;5-L (D). Blue color indicates towards positive charge, while red color denotes negative charge. Majority of the residues at the pore region are negatively charged residues. Key amino acid residues or changes at the pore entrance have been marked.
Fig. 5. SNPs identified in OsHKT1;5 in 3K-rice genomes (3K-RG). A, Distribution of SNPs in the OsHKT1;5 genomic sequence in 3K-RG. SYN SNP, Synonymous substitutions in exonic regions (E1, E2 and E3); Non-SYN SNP, Non-synonymous substitutions in exonic regions; SNP (NC), SNPs in intronic regions (I1 and I2). B, Circus based representation of SNPs and respective positions in OsHKT1;5 genomic sequence. SNP numbering as per IRGSP 1.0 (Chromosome 1). Outermost track represents SNPs and their respective positions (blue box at the top of the figure signifies the first polymorphic position; non-synonymous SNPs are indicated by orange boxes). Starting from outside, the second, third, fourth and fifth tracks represent the nucleotides adenine (red), thymine (blue), guanine (orange) and cytosine (green), respectively, with the height of each bar representing its frequency in the 3K-RG.
Fig. 6. Haplotyping of HKT1;5 in wild and cultivated rice. A , Only a subset of haplotypes seen in progenitor wild rice species (O. rufipogon and O. nivara) is seen in 3K-rice genomes (3K-RG). B, Haplotypes recognized with reference to 8 non-synonymous amino acid residue changes in OsHKT1;5 sequence and their distribution in 12 sub-populations (Wang W S et al, 2018) within 3K-RG [Amino acid changes indicted in bold are also referenced in Ren et al (2005)]. Haplotypes 2 (blue) and 10 (red) correspond to HKT1;5 sequences seen in salt sensitive genotype Koshihikari (also Nipponbare, IRGSP 1.0) and salt tolerant genotype Nona Bokra (Ren et al, 2005), respectively, and differ from one another in four amino acid residues indicated above. Occurrence of rare amino acid substitution in each haplotype is indicated in yellow. Haplotypes 11? 15 are heterozygous at one or more amino acid residue positions. C, Haplotype network inferred for OsHKT1;5 for the 3K-RG dataset. Each circle represents a haplotype. and the size of each circle is proportional to haplotype frequency in the population.
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