Introduction

Safflower (Carthamus tinctorius L.) is a diploid (2n = 24) dicot plant in the family Asteraceae (Compositae) [1]. It is an annual plant that is predominantly self-pollinated. This herbaceous crop is adapted to hot and dry environments due to its deep root system and xerophytic spines. Therefore, it is widely cultivated in arid and semiarid regions [2]. Safflower is assumed to have been domesticated in the Fertile Cresent region over 4,000 years ago, and it has a long history of cultivation in Asia, the Mediterranean region, Europe, and the Americas [3,4,5].

Safflower is mainly grown as an oil crop, it has been cultivated for use as birdseed and as a source of oil for the paint industry [6, 7]. In some areas such as Western Europe, safflower is cultivated as a source of Safflor Yellow (SY) that is produced in the floret, and used as a natural dyestuff [8]. Safflower is valuable as an edible oil crop because it produces a large amount of oil (approx. 25% oil content in seeds). It has relatively higher polyunsaturated/saturated ratios than other edible oil, which is rich in octadecadienoic acid and contains more than 70% LA [9]. As a type of essential polyunsaturated fatty acid (PUFA), LA is vital in the dietary composition for both humans and animals. As one of the oldest sources of oil for humans worldwide, the main economic traits of cultivated safflower varieties are related to its composition proportion in LA [10, 11]. Fatty acids desaturase such as FAD2 play a crucial role in regulating the composition of fatty acids, including LA. These enzymes catalyze the desaturation reactions necessary for the synthesis of unsaturated fatty acids, from saturated or monounsaturated precursors [12]. Although, it is not a mainstream oilseed crop in today’s world, it has been cultivated widely and distributed across various geographic regions. The species diversity of safflower could also serve as an important resource for genetic breeding.

The genetic diversity and natural variations in safflower have been studied using several molecular and analytical methods in recent decades [3, 13]. More recent studies have provided molecular information for safflower including its complete chloroplast genome [14], full-length transcriptome [15], and the locations of 2,008,196 single nucleotide polymorphisms, which were identified from recombinant inbred safflower lines [16]. The results of those studies and others indicated that the genetic architecture and evolution of safflower domestication are complex [17]. Such complexity has posed challenges to safflower breeding endeavors. In the past, breeding programs have used hybridization to breed new cultivars [18] and have characterized the safflower germplasm using various molecular markers, including expressed sequence tags, inter simple sequence repeats, single nucleotide polymorphism, and simple sequence repeat markers [15, 19,20,21,22]. Genome evolution involves intricate mechanisms such as gene duplication, divergence, and selection, which shape the genetic landscape of organisms over time. Gene duplication, in particular, serves as a significant driver of genome evolution, often leading to the expansion of gene families [23, 24]. Therefore, high-quality safflower reference genome and genome evolution research can reveal genetic structure and phylogenetic details, as well as biosynthesis processes of bioactive compounds. The inaugural sequencing of the safflower cultivar Anhui-1 genome employed PacBio Sequel (Pacific Biosciences) in conjunction with the Illumina Hiseq 2500 sequencing platform. The investigation primarily targeted the biosynthetic pathways of hydroxysafflor yellow A and unsaturated fatty acid [5b). The contents of oleic acid (C18:1) and linoleic acid (C18:2) were found the highest at maturity stage. For instance, C18:1n7, C18:1n9 and C18:2n6 reached 1,776, 1,666, 1,510 µg/g DW, increased by 29.9, 5.4, and 2.6 times when compared to the early stages of grain formation, respectively. According to the data results, C18:3n3 and C18:3n6 did not belong to the high content of PUFA, and their contents decreased first and then increased in the seed developmental stage. In addition to this, most of the fatty acids were increased in the seeds except C14:1, which was decreased. The composition and content of fatty acids in safflower seeds during seed development indicated that the synthesis and accumulation of polyunsaturated fatty acids C18:2 was the main factor determining the oil quality of safflower seeds.

To gain a better understanding of the relationship between genes and fatty acids species, the Pearson correlation test was performed for the intensity of fatty acids and the expression pattern of genes during the safflower seeds development stage. Our results showed that a total of 28 genes were significantly correlated with C18:1, C18:2 and C18:3 molecular species metabolites that exhibit a Pearson correlation coefficient > 0.7 and p-value < 0.05. Among them, expression pattern of 15 FAD2 genes (Cti _chr11_01896, Cti_chr9_01626, Cti_chr11_01899, Cti_chr11_01897, Cti_ chr9_01627, Cti_chr11_01898, Cti_chr9_01634, Cti_chr9_01616, Cti_chr9_01625, Cti_chr9_01617, Cti_chr3_02112, Cti_chr3_02111, Cti_chr11_01894, Cti_chr10_00208, Cti_chr4_00382) and 4 FAD6 genes (Cti_chr11_01893, Cti_chr7_00474, Cti_chr11_01895, Cti_chr3_02287) were positively correlated with C18:1n7, C18:1n9 and C18:2n6 composition patterns during seed develo** stages (Fig. 6). Importantly, two FAD6 genes Cti_chr11_01893 and Cti_chr11_01895 expression patterns showed significant correlation with C18:2 contents during seed development stage. These results indicated that FAD2 and FAD6 genes appear to be responsible for the high proportion of C18:2 in develo** safflower seeds.

Fig. 5
figure 5

Fatty acids biosynthesis and contents of seed lipids. (a) Fatty acid and oil biosynthesis in safflower. KAS II, β-ketoacyl-ACP synthetase; SAD, stromal stearoyl-ACP desaturase; FATA, acyl-ACP thioesterase; G3P, glycerol-3-phosphate; GPAT, glycerol-3-phosphate acyltransferase; LPA, lysophosphatidic acid; LPAAT, Lysophosphatidic acid acyltransferase; PA, phosphatidic acid; FAD2/3/6/7, Fatty acid desaturase; DAG, diglycerides; TAG, triglycerides; (b) Fatty acids contents of seed storage lipids in different develo** stages

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Fig. 6
figure 6

Correlation coefficient between gene expression level and contents of fatty acids. * p < 0.05

Full size image

Discussion

In the present study, we report the complete genome sequence of an economically important crop safflower. We presented valuable insights into the genetic organization of safflower, which facilitates the identification of key functional genes implicated in fatty acid synthesis. These valuable genomic resources could be easily accessible to researchers in the field for future functional and molecular breeding studies. Previous studies on the Compositae have reported genome sequences for H. annuus [31], lettuce (Lactuca sativa) [

Data availability

The raw sequence reads were deposited in China National GeneBank DataBase (CNGB db) under Project No. CNP0004859 and CNP0004861.

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Acknowledgements

This work was supported by China National GeneBank (CNGB).

Funding

This research was funded by The Science and Technology Development Project of Jilin province (20210402044GH, 20220101354JC), Science and Technology Research Project of the Education Department of Jilin Province (JJKH20220325KJ).

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Author notes

  1. Yuanyuan Dong and **aojie Wang Contribute equally to this work.

Authors and Affiliations

  1. Engineering Research Center of Bioreactor and Pharmaceutical Development, College of Life Sciences, Ministry of Education, Jilin Agricultural University, Changchun, 130118, China

    Yuanyuan Dong, Naveed Ahmad, Yepeng Sun, Yuanxin Wang, **uming Liu, Na Yao, Yang **g, Linna Du, **aowei Li, Nan Wang, Weican Liu & Fawei Wang

  2. School of Pharmaceutical Science, Key Laboratory of Biotechnology and Pharmaceutical Engineering of Zhejiang Province, Wenzhou Medical University, Wenzhou, 325035, China

    **aojie Wang & **aokun Li

  3. Sanya Nanfan Research Institute of Hainan University, Sanya, 572025, China

    Haiyan Li

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Contributions

Y.D., X.W., X.L., and H.L. performed some data analyses. J.Y., N.Y. and L.D. managed samples and tissues. Y.W. prepared materials and uploaded data. Y.D., X.W., X.L., and J.Y. performed some data analyses and prepared graphics. N.Y., X.L., N.W., X.L., and W.L., prepared the libraries. H.L., and X.L. assisted in data analysis and in the overall design of the project. F.W., H.L., and X.L. developed the figure of the study and assisted with manuscript preparation. Y.D., X.W., N.A. Y.S. X.L., J.Y., F.W., and H.L. wrote and revised the manuscript. All of the authors reviewed and approved the final manuscript.

Corresponding author

Correspondence to Haiyan Li.

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No specific approval was required for voucher specimens for this study. Voucher specimens were prepared and deposited at the Jilin agricultural University. Yuanyuan Dong and **aojie Wang undertook the identification work of the plant material. The authors have complied with all relevant institutional and national guidelines and legislation in experimental research and field studies on plants, including the collection of plant materials for this study.

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Dong, Y., Wang, X., Ahmad, N. et al. The Carthamus tinctorius L. genome sequence provides insights into synthesis of unsaturated fatty acids. BMC Genomics 25, 510 (2024). https://doi.org/10.1186/s12864-024-10405-z

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