Identification of miRNAs and Their Targets Involved in Flower and Fruit Development across Domesticated and Wild Capsicum Species
Abstract
:1. Introduction
2. Results
2.1. Analysis of Small RNAs in Pepper
2.2. Identification of Known and Novel miRNAs in Pepper
2.3. Expression Pattern of Known and Novel miRNAs in Pepper
2.4. Prediction of Putative Targets for Known and Novel miRNAs in Pepper
2.5. Expression Profile of miRNA Target Genes in C. annuum
2.6. Validation of miRNA and Target Gene Expression
3. Discussion
3.1. Role of miRNAs and Their Regulators in Flowering across Capsicum Species
3.2. Role of miRNAs and Their Regulators in Pepper Fruit Development
4. Materials and Methods
4.1. Plant Materials
4.2. Construction and Sequencing of Small RNA Libraries
4.3. Bioinformatics Analysis of miRNAs
4.4. Analysis of Differentially Expressed miRNAs
4.5. Prediction of miRNA Targets and Enrichment Analyses
4.6. Quantitative RT-qPCR and Stem-Loop RT-qPCR
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Capsicum baccatum | Capsicum annuum | Capsicum chacoense | Capsicum eximium | ||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Name | Flowering | Small Fruit | Middle Fruit | Flowering | Small Fruit | Middle Fruit | Flowering | Small Fruit | Middle Fruit | Flowering | Small Fruit | Middle Fruit | miRNA Sequence |
miR156 | 20 | 10 | 25 | 10 | 0 | 6 | 6 | 5 | 0 | 9 | 7 | 9 | UGACAGAAGAGAGUGAGCAC |
miR157 | 47 | 12 | 0 | 281 | 0 | 0 | 0 | 0 | 68 | 132 | 0 | 9 | UUGACAGAAGAUAGAGAGCAC |
miR159 | 7417 | 32107 | 22478 | 10667 | 3720 | 2206 | 578 | 1893 | 1419 | 6182 | 3176 | 3912 | UUUGGAUUGAAGGGAGCUCUA |
miR160 | 0 | 36 | 30 | 31 | 0 | 0 | 0 | 0 | 19 | 14 | 0 | 0 | UGCCUGGCUCCCUGUAUGCCA |
miR162 | 26 | 733 | 1252 | 385 | 260 | 262 | 6 | 30 | 19 | 187 | 7 | 45 | UCGAUAAACCUCUGCAUCCAG |
miR164 | 194 | 55 | 598 | 377 | 52 | 334 | 25 | 123 | 1422 | 83 | 86 | 204 | UGGAGAAGCAGGGCACGUGC |
miR165 | 31 | 17 | 14 | 7 | 0 | 0 | 0 | 0 | 6 | 0 | 0 | 35 | GUUGAGGGGAAUGUUGUCUGG |
miR166a | 1699 | 7225 | 7342 | 2025 | 729 | 815 | 383 | 1498 | 1167 | 1234 | 1523 | 1477 | UCGGACCAGGCUUCAUUCCCC |
miR166 | 0 | 16 | 25 | 1718 | 313 | 0 | 29 | 183 | 24 | 713 | 624 | 631 | GGGGAAUGUUGUCUGGCUCG |
miR167 | 116 | 354 | 725 | 302 | 8 | 44 | 0 | 29 | 7 | 0 | 16 | 51 | UGAAGCUGCCAGCAUGAUCUA |
miR168 | 11 | 46 | 79 | 32 | 10 | 52 | 0 | 0 | 0 | 35 | 0 | 13 | CCCGCCUUGCAUCAACUGAAU |
miR171 | 77 | 363 | 495 | 372 | 102 | 42 | 0 | 38 | 6 | 106 | 26 | 41 | UAUUGGCCUGGUUCACUCAGA |
miR172 | 68 | 21 | 15 | 108 | 0 | 8 | 11 | 0 | 15 | 34 | 0 | 0 | AGAAUCUUGAUGAUGCUGCAU |
miR319 | 2098 | 403 | 121 | 4461 | 154 | 90 | 290 | 126 | 54 | 2027 | 604 | 484 | UUGGACUGAAGGGAGCUCCC |
miR390 | 320 | 305 | 197 | 92 | 8 | 0 | 0 | 0 | 0 | 45 | 0 | 0 | AAGCUCAGGAGGGAUAGCGC |
miR394 | 29 | 303 | 193 | 118 | 19 | 0 | 0 | 8 | 0 | 38 | 0 | 0 | UUGGCAUUCUGUCCACCUCC |
miR395 | 106 | 26 | 17 | 63 | 0 | 41 | 0 | 44 | 45 | 107 | 0 | 0 | CUGAAGUGUUUGGGGGAACUC |
miR396 | 144 | 2668 | 3232 | 778 | 507 | 1681 | 9 | 282 | 351 | 292 | 27 | 144 | UUCCACAGCUUUCUUGAACUG |
miR398 | 25 | 20 | 428 | 641 | 0 | 79 | 0 | 196 | 20 | 1618 | 0 | 3520 | UGUGUUCUCAGGUCACCCCUU |
miR403 | 123 | 1819 | 1584 | 35 | 235 | 235 | 0 | 55 | 53 | 254 | 14 | 86 | UUAGAUUCACGCACAAACUCG |
miR408 | 0 | 7 | 117 | 0 | 0 | 38 | 0 | 0 | 8 | 110 | 147 | 79 | UGCACUGCCUCUUCCCUGGCU |
miR6478 | 2750 | 15436 | 2122 | 10213 | 6236 | 4524 | 1001 | 3789 | 1508 | 9530 | 2404 | 4669 | CCGACCUUAGCUCAGUUGGUAGA |
Capsicum baccatum | Capsicum annuum | Capsicum chacoense | Capsicum eximium | |||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Name | MFE | Flowering | Small Fruit | Middle Fruit | Flowering | Small Fruit | Middle Fruit | Flowering | Small Fruit | Middle Fruit | Flowering | Small Fruit | Middle Fruit | miRNA Sequence |
miR01 | −18.8 | 57 | 11265 | 465 | 9 | 0 | 0 | 0 | 11 | 0 | 231 | 236 | 89 | AACCCUGAACCCUGAACCCU |
miR02 | −30.7 | 11 | 85 | 11380 | 0 | 0 | 15 | 0 | 0 | 0 | 0 | 61 | 253 | AGGGAUGGCCUUGGCUCAGC |
miR03 | −49.9 | 158 | 120 | 1468 | 54 | 30 | 29 | 126 | 126 | 172 | 102 | 214 | 86 | GAAGUCCUCGUGUUGCAUCCCU |
miR04 | −47.9 | 0 | 252 | 23 | 26 | 36 | 19 | 0 | 0 | 0 | 25 | 0 | 0 | GACUAGGACGGUCUGAGGCUU |
miR05 | −46.3 | 1252 | 12908 | 32 | 640 | 568 | 432 | 92 | 214 | 60 | 402 | 137 | 130 | GCACCAGUGGUCUAGUGGUAGAAU |
miR06 | −18.3 | 75 | 715 | 584 | 359 | 183 | 131 | 8 | 122 | 38 | 381 | 36 | 136 | GCCCGUCUAGCUCAGUUGGUAGA |
miR07 | −62.6 | 7487 | 0 | 10012 | 2965 | 0 | 2156 | 4328 | 0 | 14605 | 6921 | 4728 | 5898 | GCCGGCCGGGGGACGGACUG |
miR08 | −56.1 | 0 | 55 | 592 | 17 | 0 | 12 | 0 | 22 | 66 | 49 | 13 | 35 | GCCGUCUUAGCUCAGCGGUA |
miR09 | −30.3 | 0 | 89 | 1532 | 68 | 90 | 48 | 0 | 0 | 320 | 165 | 0 | 0 | GCCGUCUUAGCUCAGUGGUAGAGC |
miR10 | −30.8 | 865 | 3358 | 64 | 416 | 0 | 0 | 62 | 452 | 0 | 654 | 389 | 309 | GCGCCUGUAGCUCAGUGGAUA |
miR11 | −44.8 | 0 | 42 | 1827 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | GCGGAAGAUCCUGAAUUUGAGACU |
miR12 | −23.7 | 239 | 530 | 8656 | 194 | 215 | 173 | 268 | 148 | 0 | 274 | 217 | 150 | GCGGGGAUAGCUCAGUUGGGAGA |
miR13 | −27.6 | 7777 | 18 | 140 | 6089 | 4959 | 2735 | 4746 | 9380 | 705 | 7712 | 8554 | 8715 | GCGUCUGUAGUCCAACGGUUAGG |
miR14 | −26.5 | 1317 | 8787 | 118 | 7068 | 18987 | 16637 | 1832 | 4800 | 9219 | 11268 | 421 | 2526 | GCUCAGUGGUAGAGCAUUUGACU |
miR15 | −37 | 1854 | 2927 | 265 | 1155 | 549 | 314 | 1232 | 2325 | 2893 | 2456 | 1162 | 1624 | GGAUGCGAUCAUACCAGCACU |
miR16 | −34.3 | 697 | 543 | 3629 | 224 | 125 | 0 | 754 | 750 | 550 | 340 | 742 | 371 | GGGAAGUCCUCGUGUUGCAUCCCU |
miR17 | −29.7 | 539 | 468 | 21 | 609 | 131 | 148 | 121 | 383 | 302 | 753 | 128 | 288 | GGGAUUGUAGUUCAAUCGGUCAGA |
miR18 | −15.9 | 0 | 0 | 4668 | 0 | 493 | 772 | 0 | 0 | 1690 | 0 | 0 | 0 | GGGGAUGUAGCUCAAAUGGU |
miR19 | −18.1 | 8955 | 3485 | 0 | 1592 | 0 | 0 | 7949 | 8286 | 0 | 3517 | 10077 | 7444 | GGGGAUGUAGCUCAAAUGGUAGA |
miR20 | −23 | 0 | 0 | 0 | 0 | 1815 | 1882 | 0 | 0 | 6380 | 5022 | 0 | 0 | GGGGAUGUAGCUCAGAUGGUA |
miR21 | −24.9 | 11206 | 4473 | 0 | 3305 | 0 | 0 | 14304 | 13268 | 0 | 0 | 16839 | 12566 | GGGGAUGUAGCUCAGAUGGUAGA |
miR22 | −55.1 | 210 | 501 | 456 | 455 | 312 | 0 | 190 | 321 | 413 | 1032 | 118 | 372 | GUCGAUAUGUCCGAGUGGUUAAGG |
miR23 | −50.5 | 1781 | 2755 | 12 | 1676 | 811 | 726 | 771 | 1077 | 1094 | 2750 | 1114 | 1937 | GUGGACGUGCCGGAGUGGUUAUC |
miR24 | −40.6 | 50 | 0 | 0 | 56 | 11 | 0 | 31 | 33 | 32 | 89 | 68 | 60 | GUGGGCGUGCCGGAGUGGUUAUC |
miR25 | −36.6 | 0 | 0 | 0 | 0 | 0 | 0 | 285 | 103 | 115 | 0 | 143 | 0 | UAGUGGUAUGAUUCUCGCUU |
miR26 | −37.8 | 98 | 0 | 0 | 0 | 238 | 112 | 438 | 235 | 0 | 429 | 668 | 159 | UAGUGGUCAGGACAUUGGACU |
miR27 | −30 | 0 | 270 | 62 | 33 | 0 | 0 | 0 | 0 | 0 | 20 | 0 | 0 | UCACCAUCUUUCGGCUGAGAUU |
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Lopez-Ortiz, C.; Peña-Garcia, Y.; Bhandari, M.; Abburi, V.L.; Natarajan, P.; Stommel, J.; Nimmakayala, P.; Reddy, U.K. Identification of miRNAs and Their Targets Involved in Flower and Fruit Development across Domesticated and Wild Capsicum Species. Int. J. Mol. Sci. 2021, 22, 4866. https://doi.org/10.3390/ijms22094866
Lopez-Ortiz C, Peña-Garcia Y, Bhandari M, Abburi VL, Natarajan P, Stommel J, Nimmakayala P, Reddy UK. Identification of miRNAs and Their Targets Involved in Flower and Fruit Development across Domesticated and Wild Capsicum Species. International Journal of Molecular Sciences. 2021; 22(9):4866. https://doi.org/10.3390/ijms22094866
Chicago/Turabian StyleLopez-Ortiz, Carlos, Yadira Peña-Garcia, Menuka Bhandari, Venkata Lakshmi Abburi, Purushothaman Natarajan, John Stommel, Padma Nimmakayala, and Umesh K. Reddy. 2021. "Identification of miRNAs and Their Targets Involved in Flower and Fruit Development across Domesticated and Wild Capsicum Species" International Journal of Molecular Sciences 22, no. 9: 4866. https://doi.org/10.3390/ijms22094866