FUNCTIONAL GAIN OF FRUIT NETTED-CRACKING IN AN INTROGRESSION LINE OF TOMATO WITH HIGHER EXPRESSION OF THE FNC GENE
Chunli ZHANG, Taotao WANG, Jing LI, Danqiu ZHANG, Qingmin XIE, Shoaib MUNIR, Jie YE, Hanxia LI, Yongen LU, Changxian YANG, Bo OUYANG, Yuyang ZHANG, Junhong ZHANG, Zhibiao YE
FUNCTIONAL GAIN OF FRUIT NETTED-CRACKING IN AN INTROGRESSION LINE OF TOMATO WITH HIGHER EXPRESSION OF THE FNC GENE
• A novel netted-cracking fruit phenotype was discovered in tomato introgression line IL4-4.
• A single dominant gene (FNC) determined the fruit netted-cracking phenotype.
• The high transcript level of FNC results in the functional gain of fruit netted-cracking and it was found to be a common mechanism in a diverse range of plant species.
Fruit cracking is a major disorder that affects the integrity of fruit and reduces the commercial value of tomato and other fleshy fruit. Here, we have found a novel fruit ‘netted-cracking’ (FNC) phenotype in tomato introgression line IL4-4 which is present in neither the donor parent (LA0716) nor the receptor parent (M82). An F2 population was generated by crossing IL4-4 with M82 to genetically characterize the FNC gene and this showed that a single dominant gene determined fruit netted-cracking. Further map-based cloning narrowed down the FNC locus to a 230 kb region on chromosome 4. Sequencing and annotation analysis show that FNC (Solyc04 g082540) was the most likely candidate gene. Functional characterization of FNC by overexpressing FNCAC and FNCIL4-4 resulted in the fruit netted-cracking phenotype, suggesting that the FNC transcript level results in the functional gain of fruit netted-cracking. These findings were further confirmed by FNC ortholog in netted-cracking pepper and melon, indicating a common regulatory mechanism in different plant species. Furthermore, cytoplasm and nucleus-localized FNC indicates increased expression of genes involved in suberin, lignin, lipid transport and cell wall metabolism. These findings provide novel genetic insights into fruit netted-cracking and offer a way to promote molecular improvement toward cracking resistant cultivars.
fine mapping / fruit netted-cracking / introgression line / transcript level
[1] |
Khadivi-Khub A. Physiological and genetic factors influencing fruit cracking. Acta Physiologiae Plantarum, 2015, 37(1): 1718
CrossRef
Google scholar
|
[2] |
Capel C, Yuste-Lisbona F J, López-Casado G, Angosto T, Cuartero J, Lozano R, Capel J. Multi-environment QTL mapping reveals genetic architecture of fruit cracking in a tomato RIL Solanum lycopersicum × S. pimpinellifolium population. Theoretical and Applied Genetics, 2017, 130(1): 213–222
CrossRef
Pubmed
Google scholar
|
[3] |
Islam M Z, Mele M A, Baek J P, Kang H M. Cherry tomato qualities affected by foliar spraying with boron and calcium. Horticulture, Environment and Biotechnology, 2016, 57(1): 46–52
CrossRef
Google scholar
|
[4] |
Knoche M, Peschel S. Water on the surface aggravates microscopic cracking of the sweet cherry fruit cuticle. Journal of the American Society for Horticultural Science, 2006, 131(2): 192–200
CrossRef
Google scholar
|
[5] |
Ginzberg I, Stern R A. Strengthening fruit-skin resistance to growth strain by application of plant growth regulators. Scientia Horticulturae, 2016, 198: 150–153
CrossRef
Google scholar
|
[6] |
Jiang H K, Tian H M, Yan C S, Jia L, Wang Y, Wang M X, Jiang C J, Li Y Y, Jiang J Y, Fang L, Zhao Q A. RNA-seq analysis of watermelon (Citrullus lanatus) to identify genes involved in fruit cracking. Scientia Horticulturae, 2019, 248: 248–255
CrossRef
Google scholar
|
[7] |
Song Y Q, Li J, Fu L J, Li N, Li L L. Change of fruit surface characteristics and its relationship with water absorption and fruit cracking in ziziphus jujuba ‘Huping’. Scientia Silvae Sinicae, 2018, 54(12): 52–59 (in Chinese)
|
[8] |
Liao N, Hu Z, Li Y, Hao J, Chen S, Xue Q, Ma Y, Zhang K, Mahmoud A, Ali A, Malangisha G K, Lyu X, Yang J, Zhang M. Ethylene-responsive factor 4 is associated with the desirable rind hardness trait conferring cracking resistance in fresh fruits of watermelon. Plant Biotechnology Journal, 2020, 18(4): 1066–1077
CrossRef
Pubmed
Google scholar
|
[9] |
Giménez E, Dominguez E, Pineda B, Heredia A, Moreno V, Lozano R, Angosto T. Transcriptional activity of the MADS box ARLEQUIN/TOMATO AGAMOUS-LIKE1 gene is required for cuticle development of tomato fruit. Plant Physiology, 2015, 168(3): 1036–1048
CrossRef
Pubmed
Google scholar
|
[10] |
Shi J X, Adato A, Alkan N, He Y, Lashbrooke J, Matas A J, Meir S, Malitsky S, Isaacson T, Prusky D, Leshkowitz D, Schreiber L, Granell A R, Widemann E, Grausem B, Pinot F, Rose J K C, Rogachev I, Rothan C, Aharoni A. The tomato SlSHINE3 transcription factor regulates fruit cuticle formation and epidermal patterning. New Phytologist, 2013, 197(2): 468–480
CrossRef
Pubmed
Google scholar
|
[11] |
Petit J, Bres C, Mauxion J P, Bakan B, Rothan C. Breeding for cuticle-associated traits in crop species: traits, targets, and strategies. Journal of Experimental Botany, 2017, 68(19): 5369–5387
CrossRef
Pubmed
Google scholar
|
[12] |
Hovav R, Chehanovsky N, Moy M, Jetter R, Schaffer A A. The identification of a gene (Cwp1), silenced during Solanum evolution, which causes cuticle microfissuring and dehydration when expressed in tomato fruit. Plant Journal, 2007, 52(4): 627–639
CrossRef
Pubmed
Google scholar
|
[13] |
Chechanovsky N, Hovav R, Frenkel R, Faigenboim A, Eselson Y, Petreikov M, Moy M, Shen S, Schaffer A A. Low temperature upregulates cwp expression and modifies alternative splicing patterns, increasing the severity of cwp-induced tomato fruit cuticular microfissures. Horticulture Research, 2019, 6(1): 122
CrossRef
Pubmed
Google scholar
|
[14] |
Cui L, Qiu Z, Wang Z, Gao J, Guo Y, Huang Z, Du Y, Wang X. Fine mapping of a gene (ER4.1) that causes epidermal reticulation of tomato fruit and characterization of the associated transcriptome. Frontiers in Plant Science, 2017, 8: 1254
CrossRef
Pubmed
Google scholar
|
[15] |
Keren-Keiserman A, Tanami Z, Shoseyov O, Ginzberg I. Peroxidase activity associated with suberization processes of the muskmelon (Cucumis melo) rind. Physiologia Plantarum, 2004, 121(1): 141–148
CrossRef
Pubmed
Google scholar
|
[16] |
Ramamurthy R K, Waters B M. Identification of fruit quality and morphology QTLs in melon (Cucumis melo) using a population derived from flexuosus and cantalupensis botanical groups. Euphytica, 2015, 204(1): 163–177
CrossRef
Google scholar
|
[17] |
Wang Y Z, Dai M S, Cai D Y, Zhang S J, Shi Z B. A review for the molecular research of russet/semi-russet of sand pear exocarp and their genetic characters. Scientia Horticulturae, 2016, 210: 138–142
CrossRef
Google scholar
|
[18] |
Yasuzumi G, Sugihara R. The fine structure of nuclei fixed by a double fixation procedure. Experimental Cell Research, 1964, 33(3): 578–580
CrossRef
Pubmed
Google scholar
|
[19] |
Monforte A J, Friedman E, Zamir D, Tanksley S D. Comparison of a set of allelic QTL-NILs for chromosome 4 of tomato: deductions about natural variation and implications for germplasm utilization. Theoretical and Applied Genetics, 2001, 102(4): 572–590
CrossRef
Google scholar
|
[20] |
Bard F, Casano L, Mallabiabarrena A, Wallace E, Saito K, Kitayama H, Guizzunti G, Hu Y, Wendler F, Dasgupta R, Perrimon N, Malhotra V. Functional genomics reveals genes involved in protein secretion and Golgi organization. Nature, 2006, 439(7076): 604–607
CrossRef
Pubmed
Google scholar
|
[21] |
Saladié M, Matas A J, Isaacson T, Jenks M A, Goodwin S M, Niklas K J, Xiaolin R, Labavitch J M, Shackel K A, Fernie A R, Lytovchenko A, O’Neill M A, Watkins C B, Rose J K C. A reevaluation of the key factors that influence tomato fruit softening and integrity. Plant Physiology, 2007, 144(2): 1012–1028
CrossRef
Pubmed
Google scholar
|
[22] |
Isaacson T, Kosma D K, Matas A J, Buda G J, He Y, Yu B, Pravitasari A, Batteas J D, Stark R E, Jenks M A, Rose J K C. Cutin deficiency in the tomato fruit cuticle consistently affects resistance to microbial infection and biomechanical properties, but not transpirational water loss. Plant Journal, 2009, 60(2): 363–377
CrossRef
Pubmed
Google scholar
|
[23] |
Hen-Avivi S, Lashbrooke J, Costa F, Aharoni A. Scratching the surface: genetic regulation of cuticle assembly in fleshy fruit. Journal of Experimental Botany, 2014, 65(16): 4653–4664
CrossRef
Pubmed
Google scholar
|
[24] |
Jiang F, Lopez A, Jeon S, de Freitas S T, Yu Q, Wu Z, Labavitch J M, Tian S, Powell A L T, Mitcham E. Disassembly of the fruit cell wall by the ripening-associated polygalacturonase and expansin influences tomato cracking. Horticulture Research, 2019, 6(1): 17
CrossRef
Pubmed
Google scholar
|
[25] |
Correia S, Schouten R, Silva A P, Gonçalves B. Sweet cherry fruit cracking mechanisms and prevention strategies: a review. Scientia Horticulturae, 2018, 240: 369–377
CrossRef
Google scholar
|
[26] |
Cohen H, Dong Y, Szymanski J, Lashbrooke J, Meir S, Almekias-Siegl E, Zeisler-Diehl V V, Schreiber L, Aharoni A. A multilevel study of melon fruit reticulation provides insight into skin ligno-suberization hallmarks. Plant Physiology, 2019, 179(4): 1486–1501
CrossRef
Pubmed
Google scholar
|
[27] |
Pollard M, Beisson F, Li Y, Ohlrogge J B. Building lipid barriers: biosynthesis of cutin and suberin. Trends in Plant Science, 2008, 13(5): 236–246
CrossRef
Pubmed
Google scholar
|
[28] |
Lashbrooke J, Aharoni A, Costa F. Genome investigation suggests MdSHN3, an APETALA2-domain transcription factor gene, to be a positive regulator of apple fruit cuticle formation and an inhibitor of russet development. Journal of Experimental Botany, 2015, 66(21): 6579–6589
CrossRef
Pubmed
Google scholar
|
[29] |
Lashbrooke J, Cohen H, Levy-Samocha D, Tzfadia O, Panizel I, Zeisler V, Massalha H, Stern A, Trainotti L, Schreiber L, Costa F, Aharoni A. MYB107 and MYB9 homologs regulate suberin deposition in angiosperms. Plant Cell, 2016, 28(9): 2097–2116
CrossRef
Pubmed
Google scholar
|
[30] |
Xing Y L, Shi C X, Li H X, Ye Z B. Formation mechanism of tomato fruit cuticles. Acta Horticulturae Sinica, 2016, 43(9): 1726–1734 (in Chinese)
|
[31] |
España L, Heredia-Guerrero J A, Reina-Pinto J J, Fernández-Muñoz R, Heredia A, Domínguez E. Transient silencing of CHALCONE SYNTHASE during fruit ripening modifies tomato epidermal cells and cuticle properties. Plant Physiology, 2014, 166(3): 1371–1386
CrossRef
Pubmed
Google scholar
|
[32] |
Fich E A, Segerson N A, Rose J K C. The plant polyester cutin: biosynthesis, structure, and biological roles. Annual Review of Plant Biology, 2016, 67(1): 207–233
CrossRef
Pubmed
Google scholar
|
[33] |
Kolattukudy P E. Biopolyester membranes of plants: cutin and suberin. Science, 1980, 208(4447): 990–1000
CrossRef
Pubmed
Google scholar
|
[34] |
Pighin J A, Zheng H, Balakshin L J, Goodman I P, Western T L, Jetter R, Kunst L, Samuels A L. Plant cuticular lipid export requires an ABC transporter. Science, 2004, 306(5696): 702–704
CrossRef
Pubmed
Google scholar
|
/
〈 | 〉 |