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A number of cis-regulatory elements (CREs) conserved during evolution have been found to be responsible for phenotypic novelty and variation. Cucurbit crops such as cucumber (Cucumis sativus), watermelon (Citrullus lanatus), melon (Cucumis melo), and squash (Cucurbita maxima) develop fruits from an inferior ovary and share some similar biological processes during fruit development. Whether conserved regulatory sequences play critical roles in fruit development of cucurbit crops remains to be explored. In six well-studied cucurbit species, we identified 392,438 conserved noncoding sequences (CNSs), including 82,756 that are specific to cucurbits, by comparative genomics. Genome-wide profiling of accessible chromatin regions (ACRs) and gene expression patterns mapped 20,865 to 43,204 ACRs and their potential target genes for two fruit tissues at two key developmental stages in six cucurbits. Integrated analysis of CNSs and ACRs revealed 4,431 syntenic orthologous CNSs, including 1,687 cucurbit-specific CNSs that overlap with ACRs that are present in all six cucurbit crops and that may regulate the expression of 757 adjacent orthologous genes. CRISPR mutations targeting two CNSs present in the 1,687 cucurbit-specific sequences resulted in substantially altered fruit shape and gene expression patterns of adjacent NAC1 (NAM, ATAF1/2, and CUC2) and EXT-like (EXTENSIN-like) genes, validating the regulatory roles of these CNSs in fruit development. These results not only provide a number of target CREs for cucurbit crop improvement, but also provide insight into the roles of CREs in plant biology and during evolution.

Competing Interests: Conflict of interest statement. None declared.

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Titel:	Identification and functional characterization of conserved cis-regulatory elements responsible for early fruit development in cucurbit crops.
Autor/in / Beteiligte Person:	Xin, H ; Liu, X ; Chai, S ; Yang, X ; Li, H ; Wang, B ; Xu, Y ; Lin, S ; Zhong, X ; Liu, B ; Lu, Z ; Zhang, Z
Zeitschrift:	The Plant cell, Jg. 36 (2024-05-29), Heft 6, S. 2272-2288
Veröffentlichung:	2021- : [Oxford] : Oxford University Press ; <i>Original Publication</i>: Rockville, MD : American Society of Plant Physiologists, c1989-, 2024
Medientyp:	academicJournal
ISSN:	1532-298X (electronic)
DOI:	10.1093/plcell/koae064
Schlagwort:	Regulatory Sequences, Nucleic Acid genetics Crops, Agricultural genetics Crops, Agricultural growth & development Cucurbita genetics Cucurbita growth & development Citrullus genetics Citrullus growth & development Citrullus metabolism Cucumis sativus genetics Cucumis sativus growth & development Plant Proteins genetics Plant Proteins metabolism Genome, Plant genetics Fruit genetics Fruit growth & development Gene Expression Regulation, Plant Conserved Sequence
Sonstiges:	Nachgewiesen in: MEDLINE Sprachen: English Publication Type: Journal Article Language: English [Plant Cell] 2024 May 29; Vol. 36 (6), pp. 2272-2288. MeSH Terms: Fruit* / genetics ; Fruit* / growth & development ; Gene Expression Regulation, Plant* ; Conserved Sequence* ; Regulatory Sequences, Nucleic Acid / genetics ; Crops, Agricultural / genetics ; Crops, Agricultural / growth & development ; Cucurbita / genetics ; Cucurbita / growth & development ; Citrullus / genetics ; Citrullus / growth & development ; Citrullus / metabolism ; Cucumis sativus / genetics ; Cucumis sativus / growth & development ; Plant Proteins / genetics ; Plant Proteins / metabolism ; Genome, Plant / genetics References: Bioinformatics. 2014 Apr 1;30(7):923-30. (PMID: 24227677) ; Cell. 2021 Apr 1;184(7):1724-1739.e16. (PMID: 33667348) ; Nat Commun. 2017 Feb 06;8:14229. (PMID: 28165450) ; Nat Plants. 2018 Oct;4(10):784-791. (PMID: 30250279) ; Science. 2019 Sep 20;365(6459):1291-1295. (PMID: 31604238) ; J Exp Bot. 2014 Aug;65(16):4625-37. (PMID: 24520021) ; New Phytol. 2023 Jul;239(1):364-373. (PMID: 36967583) ; J Exp Bot. 2013 Nov;64(14):4541-57. (PMID: 24023249) ; Mol Biol Evol. 2000 Apr;17(4):540-52. (PMID: 10742046) ; Nat Commun. 2018 Nov 9;9(1):4734. (PMID: 30413711) ; Nat Ecol Evol. 2018 Jan;2(1):152-163. (PMID: 29180706) ; Plant Physiol. 2010 May;153(1):80-98. (PMID: 20335402) ; Hortic Res. 2022 Jan 20;:. (PMID: 35048122) ; Genome Biol. 2014;15(12):550. (PMID: 25516281) ; Genome Res. 2005 Aug;15(8):1034-50. (PMID: 16024819) ; Theor Appl Genet. 2020 Jan;133(1):1-21. (PMID: 31768603) ; Genome Res. 2004 Apr;14(4):708-15. (PMID: 15060014) ; Proc Natl Acad Sci U S A. 2010 Aug 10;107(32):14269-73. (PMID: 20656934) ; Bioinformatics. 2007 Jan 15;23(2):257-8. (PMID: 17098774) ; Plant Physiol. 2010 Feb;152(2):553-65. (PMID: 20018602) ; Bioinformatics. 2018 Sep 1;34(17):i884-i890. (PMID: 30423086) ; Mol Biol Evol. 2007 Aug;24(8):1586-91. (PMID: 17483113) ; Hortic Res. 2018 Dec 21;5:75. (PMID: 30588320) ; Nat Commun. 2019 Nov 14;10(1):5158. (PMID: 31727887) ; J Exp Bot. 2020 Jun 22;71(12):3560-3574. (PMID: 32338291) ; BMC Genomics. 2008 Jun 05;9:275. (PMID: 18534026) ; Science. 2022 Mar 25;375(6587):eabg7985. (PMID: 35324310) ; Nat Plants. 2019 Dec;5(12):1237-1249. (PMID: 31740773) ; Cell. 2017 Oct 5;171(2):470-480.e8. (PMID: 28919077) ; Plant Mol Biol. 2019 May;100(1-2):151-161. (PMID: 30840202) ; Nat Plants. 2019 Dec;5(12):1250-1259. (PMID: 31740772) ; Front Plant Sci. 2022 Jun 10;13:878037. (PMID: 35755703) ; Brief Bioinform. 2011 Jan;12(1):41-51. (PMID: 21278375) ; Plant Cell Physiol. 2002 Dec;43(12):1421-35. (PMID: 12514239) ; Cell. 2014 Oct 9;159(2):374-387. (PMID: 25303531) ; Trends Plant Sci. 2016 Jun;21(6):506-515. (PMID: 26876195) ; Science. 2019 Nov 8;366(6466):. (PMID: 31488704) ; Hortic Res. 2023 Jan 30;10(3):uhad007. (PMID: 36960430) ; Bioinformatics. 2016 Oct 1;32(19):3047-8. (PMID: 27312411) ; Genome Res. 2003 Sep;13(9):2178-89. (PMID: 12952885) ; Curr Opin Plant Biol. 2007 Jun;10(3):283-9. (PMID: 17442612) ; Genome Biol. 2008;9(9):R137. (PMID: 18798982) ; Nat Methods. 2012 Mar 04;9(4):357-9. (PMID: 22388286) ; Bioinformatics. 2015 Jul 15;31(14):2382-3. (PMID: 25765347) ; J Integr Plant Biol. 2022 Jul;64(7):1448-1461. (PMID: 35568969) ; Nat Rev Genet. 2019 Apr;20(4):207-220. (PMID: 30675018) ; Annu Rev Plant Biol. 2023 May 22;74:111-137. (PMID: 36608347) ; Plant Cell. 2019 May;31(5):1063-1076. (PMID: 30914499) ; Nat Rev Genet. 2013 Dec;14(12):840-52. (PMID: 24240513) ; Genome Biol. 2019 Dec 16;20(1):278. (PMID: 31842956) ; Nat Plants. 2018 Dec;4(12):1102-1111. (PMID: 30420712) ; Cell. 2021 Mar 4;184(5):1362-1376.e18. (PMID: 33545087) ; Science. 2020 Nov 6;370(6517):. (PMID: 33154111) ; Plant Cell. 2021 May 5;33(3):475-491. (PMID: 33955490) ; Dev Cell. 2020 Sep 28;54(6):742-757.e8. (PMID: 32755547) ; Mol Biol Evol. 2015 Jan;32(1):268-74. (PMID: 25371430) ; Nucleic Acids Res. 2014 Jul;42(Web Server issue):W187-91. (PMID: 24799436) ; Methods. 2001 Dec;25(4):402-8. (PMID: 11846609) ; Plant Cell. 2018 Jan;30(1):15-36. (PMID: 29229750) ; Plant Cell. 2022 Feb 3;34(2):718-741. (PMID: 34918159) ; Nat Methods. 2015 Apr;12(4):357-60. (PMID: 25751142) ; Plant Cell. 2019 Jun;31(6):1289-1307. (PMID: 30979795) ; Bioinformatics. 2009 Aug 15;25(16):2078-9. (PMID: 19505943) ; Brief Bioinform. 2013 Mar;14(2):178-92. (PMID: 22517427) ; Nucleic Acids Res. 2004 Mar 19;32(5):1792-7. (PMID: 15034147) Grant Information: 32225044 National Natural Science Foundation of China; 2016YFD0100307 China National Key Research and Development Program for Crop Breeding; National High-level Talent Special Support Program in China; "Taishan Scholar" Foundation of the Peoples Government of Shandong Province; Chinese Academy of Agricultural Sciences Substance Nomenclature: 0 (Plant Proteins) Entry Date(s): Date Created: 20240229 Date Completed: 20240528 Latest Revision: 20240627 Update Code: 20240627 PubMed Central ID: PMC11132967

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Identification and functional characterization of conserved cis-regulatory elements responsible for early fruit development in cucurbit crops.