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

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Front. Agr. Sci. Eng. ›› 2021, Vol. 8 ›› Issue (2) : 280-291. DOI: 10.15302/J-FASE-2020374
RESEARCH ARTICLE
RESEARCH ARTICLE

FUNCTIONAL GAIN OF FRUIT NETTED-CRACKING IN AN INTROGRESSION LINE OF TOMATO WITH HIGHER EXPRESSION OF THE FNC GENE

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Highlights

• 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.

Abstract

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.

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Keywords

fine mapping / fruit netted-cracking / introgression line / transcript level

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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. Front. Agr. Sci. Eng., 2021, 8(2): 280‒291 https://doi.org/10.15302/J-FASE-2020374

References

[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

Supplementary materials

The online version of this article at https://doi.org/10.15302/J-FASE-2020374 contains supplementary materials (Figs. S1–S6; Tables S1–S3).

Acknowledgements

This work was supported by grants from the National Natural Science Foundation of China (31672149 and 31991182), the National Key Research and Development Program of China (2017YFD0101902), and CARS-23-A-03.

Compliance with ethics guidelines

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, and Zhibiao Ye declare that they have no conflicts of interest or financial conflicts to disclose. This article does not contain any studies with human or animal subjects performed by any of the authors.

RIGHTS & PERMISSIONS

The Author(s) 2020. Published by Higher Education Press. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0)
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