**1. Introduction**

Sugars Will Eventually be Exported Transporter (SWEET) is a new type of sugar transporter that was first identified in *Arabidopsis thaliana* in 2010 [1]. Comparing with monosaccharide transporters (MST) and sucrose transporters (SUT), SWEET proteins are capable of transporting sugar bidirectionally without energy dependence, and the types of substrates for sugar transport are more extensive [2]. In plants, SWEET proteins usually contain seven transmembrane helices (TMHs); two MtN3/saliva domains with three TMHs are connected by the fourth TMH to form a "3-1-3" structure [3]. The SWEET family is divided into four Clades. Different clades have different preferences for monosaccharides or disaccharides, in which Clades I and II prefer transporting hexose and Clade III prefer transporting sucrose, while SWEET proteins of Clade IV tend to transport fructose on the tonoplast [4–7].

Due to the advances in whole-genome sequencing in plants, the genome-wide identification of *SWEET* genes has been reported in many crops, vegetables, and fruits, such as rice (*Oryza sativa*) [8], soybean (*Glycine max*) [9], sorghum (*Sorghum bicolor*) [10], tomato (*Solanum lycopersicum*) [11], potato (*Solanum tuberosum*) [12], cabbage (*Brassica oleracea*) [13],

**Citation:** Song, X.; Kou, Y.; Duan, M.; Feng, B.; Yu, X.; Jia, R.; Zhao, X.; Ge, H.; Yang, S. Genome-Wide Identification of the Rose *SWEET* Gene Family and Their Different Expression Profiles in Cold Response between Two Rose Species. *Plants* **2023**, *12*, 1474. https://doi.org/ 10.3390/plants12071474

Academic Editors: Aiping Song and Yu Chen

Received: 18 December 2022 Revised: 2 March 2023 Accepted: 3 March 2023 Published: 28 March 2023

**Copyright:** © 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

tea plant (*Camellia sinensis*) [14], apple (*Malus domestica*) [15], grape (*Vitis vinifera*) [16], and banana (*Musa acuminate*) [17]. Previous studies show that *SWEET* genes in plants are involved in many biological processes, including the regulation of pollen development, nectar secretion, seed development, phloem loading, and leaf senescence. In Arabidopsis, loss of function of *AtSWEET8/RPG1* led to male sterility, indicating a key role in the maintenance of pollen viability [1,18]. *AtSWEET13* is also demonstrated to have the function for pollen development in Arabidopsis [19]. *AtSWEET9/Nec1* and its homologous genes in tobacco (*Nicotiana attenuata*) and rape (*Brassica rapa*) are proven to be essential for nectar secretion [20]. AtSWEET10 is reported to be the downstream of FLOWERING LOCUS T (FT) during floral transition in Arabidopsis [21]. AtSWEET11, 12, and 15 are beneficial to seed filling by mediating sucrose transfer from the seed coat to the endosperm [22]. AtSWEET11 and 12 are also responsible for phloem loading for long-distance transport of sucrose [7,23]. OsSWEET4, 11, and 15 in rice (*Oryza sativa*) and ZmSWEET4 in maize (*Zea mays*) are involved in the transport of hexose or sucrose in the endosperm to promote seed filling [24,25]. AtSWEET13 and 14 may be involved in modulating the GA response in Arabidopsis [26]. The NAC transcription factor ORE1 could bind to the *AtSWEET15* promoter to positively regulate leaf senescence [27]. CmSWEET17 could be involved in the process of sucrose-induced axillary bud outgrowth in chrysanthemum (*Chrysanthemum moriflorum*), possibly via the auxin transport pathway [28].

*SWEET* genes also play very important roles in response to biotic and abiotic stresses. Overexpression of *AtSWEET16* and its homologous genes in tea and apples can enhance the cold resistance of the transgenic calli or plants [14,29,30]. Moreover, overexpression of *CsSWEET1a* and *CsSWEET17* from tea also improves the cold tolerance of the transgenic Arabidopsis plants [31]. Loss of function in *AtSWEET17* may affect lateral root development and lead to impaired drought resistance [32]. *AtSWEET2* inhibits *Pythium* infection by reducing the availability of sugars in the rhizosphere of Arabidopsis seedlings [33,34]. In grape, overexpression of the *VvSWEET4* increases hexose content in hair roots and enhances resistance to *Pythium* [35]. In rice, *OsSWEET11*, *13*, and *14* are involved in resistance to bacterial blight disease by regulation of the upstream transcription factors [36–38]. However, no information about the *SWEET* gene family is known for the genus *Rosa* L.

Rose is one of the most popular flowers in the world and is widely used in cut flowers, potted flowers, garden cultivation, and essential oil production [39]. Cold stress affects the growth and distribution of plants, resulting in freezing injuries and even the death of plants [40–42]. The rose industry suffers great commercial losses every year due to cold stress [40–42]. *Rosa beggeriana* is a wild species that originated in cold and arid Central Asia, including northwest China. It has extreme cold resistance, which can be inherited through interspecific hybridization with modern rose cultivars [43]. Our previous study found that the significantly higher freezing tolerance in the shoot of *R. beggeriana* than that of *R. fortuneana*, which originated in southeastern China, might be due to the stronger ability of the spatial transfer of soluble sugars from leaves to shoots and consequently the storage of soluble sugars as starch in the shoots during overwintering [44]. The transcriptome analyses in *R. multiflora* and *R. xanthina* further indicated that the pathways of starch and sucrose metabolism were activated during cold stress [42,45]. However, it is not clear whether and which members of the SWEET gene family may participate in the cold response of a rose. Furthermore, it is not sure if there are species differences in these cold-response SWEET genes among the cold-sensitive and cold-tolerant species in *Rosa* L.

In this study, the *SWEET* family genes in rose were identified, and their gene structures, motif compositions, phylogenetic relationships, chromosome locations, gene duplications, and *cis*-acting elements were analyzed on the basis of the genome sequence of *R. chinensis* 'Old blush'. The comparison of expression patterns of the *SWEET* family genes was further investigated between *R. chinensis* 'Old blush' and *R. beggeriana* during cold treatment. Finally, the analysis of subcellular localization was conducted on the screened cold-response *RbSWEET* genes in *R. beggeriana*. Our results will contribute to a better understanding of

the *SWEET* gene family in rose and provide valuable information for further functional analysis of *RbSWEET* genes in response to cold tolerance.
