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Article

Genome-Wide Identification and Expression Analysis of JAZ Family Involved in Hormone and Abiotic Stress in Sweet Potato and Its Two Diploid Relatives

by
Zhengwei Huang
†,
Zhen Wang
†,
Xu Li
,
Shaozhen He
,
Qingchang Liu
,
Hong Zhai
,
Ning Zhao
,
Shaopei Gao
and
Huan Zhang
*
Key Laboratory of Sweet Potato Biology and Biotechnology, Ministry of Agriculture and Rural Affairs/Beijing Key Laboratory of Crop Genetic Improvement/Laboratory of Crop Heterosis & Utilization and Joint Laboratory for International Cooperation in Crop Molecular Breeding, Ministry of Education, College of Agronomy & Biotechnology, China Agricultural University, Beijing 100193, China
*
Author to whom correspondence should be addressed.
†
Zhengwei Huang and Zhen Wang are equally contributed to this work.
Int. J. Mol. Sci. 2021, 22(18), 9786; https://doi.org/10.3390/ijms22189786
Submission received: 8 August 2021 / Revised: 6 September 2021 / Accepted: 6 September 2021 / Published: 10 September 2021
(This article belongs to the Section Biochemistry)
Browse Figures
Versions Notes

Abstract

:
Jasmonate ZIM-domain (JAZ) proteins are key repressors of a jasmonic acid signaling pathway. They play essential roles in the regulation of plant growth and development, as well as environmental stress responses. However, this gene family has not been explored in sweet potato. In this study, we identified 14, 15, and 14 JAZs in cultivated hexaploid sweet potato (Ipomoea batatas, 2n = 6x = 90), and its two diploid relatives Ipomoea trifida (2n = 2x = 30) and Ipomoea triloba (2n = 2x = 30), respectively. These JAZs were divided into five subgroups according to their phylogenetic relationships with Arabidopsis. The protein physiological properties, chromosome localization, phylogenetic relationship, gene structure, promoter cis-elements, protein interaction network, and expression pattern of these 43 JAZs were systematically investigated. The results suggested that there was a differentiation between homologous JAZs, and each JAZ gene played different vital roles in growth and development, hormone crosstalk, and abiotic stress response between sweet potato and its two diploid relatives. Our work provided comprehensive comparison and understanding of the JAZ genes in sweet potato and its two diploid relatives, supplied a theoretical foundation for their functional study, and further facilitated the molecular breeding of sweet potato.

1. Introduction

Jasmonic acid (JA) plays a central role in plant growth, developmental processes, and plant response to biotic and abiotic stresses [1,2,3,4]. The crosstalks among JA and other plant hormones regulate the balance between plant growth and defense [5,6,7]. The core JA signaling module consists of the JA receptor CORONATINE INSENSITIVE 1 (COI1), which interacts with multiple proteins to form the SCFCOI1 E3 ubiquitin ligase complex, a subset of jasmonate–ZIM domain (JAZ) repressor proteins, and the various transcription factors such as MYC2 involved in regulating the expression of JA-responsive genes. In the absence of JA-Ile, the bioactive form of JA, JAZ proteins act as repressors of the transcription factors; however, the presence of JA-Ile promotes the interaction between COI1 and JAZ proteins, and the JAZ proteins are subsequently ubiquitinated by SCFCOI1 and degraded through the 26S proteasome pathway. Thus, the repression of the transcription factors is relieved, allowing them to activate the expression of JA-responsive genes [8,9,10,11,12]. Therefore, the JAZ repressor is critical in the signaling cascades triggered by jasmonates.
The JAZ family is a branch of the TIFY family that has a conserved TIF[F/Y]XG motif known as the TIFY (ZIM) domain [13]. Besides, JAZs contain a Jas (CCT2) domain with consensus sequences SLX2FX2KRX2RX5PY near its C terminal [14]. The different domains provide specific interactions for proteins. The TIFY domain could recruit TOPLESS (TPL) protein by interacting with the NOVEL INTERACTOR OF JAZ (NINJA) proteins, which contain ERF-associated amphiphilic repression (EAR) motif, and then contribute to transcriptional repression of jasmonate responses [15,16,17]. The Jas domain could interact with COI1 and transcription factors that were involved in JA signaling pathway [18]. The Arabidopsis, maize, rice, Brassica napus, Camellia sinensis, and soybean genomes encode 13, 26, 15, 52, 13, and 25 JAZs, respectively [13,19,20,21,22,23]. The JAZ proteins from different plant species could be divided naturally into different numbers of sub-groups based on their evolutionary relationship [20,21,22,23]. Recent studies have shown that individual JAZ participated in abiotic stress and hormone treatment responses. In Arabidopsis, JAZ1/4 could interact with ICE1/4 to repress freezing stress [24]. WRKY57 interacted with JAZ4/8 and IAA29 and was involved in JA-induced leaf senescence signaling pathways mediated by auxin and JA [25]. JAZ1 protein interacted with DELLA proteins which are repressors of the gibberellin (GA) pathway, to mediate the crosstalk of JA and GA [26]. Several JAZ repressors could interact with ABSCISIC ACID INSENSITIVE 3 (ABI3) to integrate JA and abscisic acid (ABA) signaling pathways during seeding germination [27]. The effector HopX1 from Pseudomonas syringae interacted with and promoted the degradation of JAZ proteins by regulating JA and salicylic acid (SA) signaling pathways [28]. In rice, more efficient activation of OsJAZ8, which was driven by the ZOS3–11 promoter, was accompanied by improved salt tolerance of the transgenic seedlings [29]. OsJAZ1 interacted with OsbHLH148 to enhance drought tolerance [30]. In soybean, GmWRKY40 interacted with JAZ proteins and response to Phytophthora sojae by modulating hydrogen peroxidase accumulation [31]. In apple, JAZ1–TRB1–MYB9 module dynamically modulated JA-mediated accumulation of anthocyanin and proanthocyanidin. However, only IbJAZ10 was characterized in sweet potato. Heterologous expression of IbJAZ10 decreased fusarium wilt resistance in tobacco [32]. Therefore, more research needs to be conducted on JAZs of sweet potato.
Sweet potato (Ipomoea batatas (L.) Lam., 2n = B1B1B2B2B2B2 = 6x = 90), belonging to the family Convolvulaceae, is an important food source for both humans and domesticated animals, as well as a new source of bioenergy in the form of bioethanol for fuel production [33]. It is widely planted in more than 100 countries or regions worldwide [34]. As sweet potato is mainly planted on marginal land, it is routinely exposed to suboptimal growth conditions, such as drought [35,36], salinity [37,38], low temperature [39,40], and oxidation [41,42], underscoring the importance of improving abiotic tolerance to maintain productivity. The sweet potato genome is large and complex due to polyploidy and a high degree of heterozygosity. In recent years, genome assemblies of a hexaploid sweet potato Taizhong 6 [43], and two diploid species closely related to the hexaploid sweet potato, Ipomoea trifida NCNSP0306 (2n = 2x = 30) and Ipomoea triloba NCNSP0323 (2n = 2x = 30) [44], were released, making it possible to identify and analyze important gene families at the whole genome level in sweet potato.
In this study, a total of 43 JAZs (i.e., 14 in I. batatas, 15 in I. trifida, and 14 in I. triloba) were identified from the cultivated hexaploid sweet potato and its two diploid relatives. They were classified into five subgroups. We systematically investigated the properties of the protein, chromosome localization, phylogenetic relationship, conserved motifs, gene structure, cis-elements of the promoter, and protein interaction network of JAZs in sweet potato. Moreover, the tissue specificity and expression pattern analysis for hormone response and abiotic stress of JAZs were analyzed by qRT-PCR and RNA-seq. The evolution, different functions on development, hormone crosstalk, and abiotic stress response were discovered between sweet potato and its two diploid relatives.

2. Results

2.1. Identification and Characteristic of JAZs in Sweet Potato and Its Two Diploid Relatives

In order to identify all JAZs in sweet potato and its two diploid relatives, three typical strategies (i.e., Blastp search, hmmersearch, SMART and CD-search databases) were employed. A total of 43 JAZs were identified in I. batatas (14), named after “Ib”; I. trifida (15), named after “Itf”; and I. triloba (14), named after “Itb”. The physicochemical properties of JAZs were analyzed using the sequences from I. batatas (Table 1). The CDS length of IbJAZs ranges from 637 bp (IbJAZ8.2) to 2118 bp (IbJAZ4), and the genomic lengths vary from 918 bp to 4050 bp. The amino acid lengths of IbJAZs range from 138 aa (IbJAZ8.2) to 384 aa (IbJAZ4), molecular weight (MW) varies from 15.585 kDa to 40.743 kDa, and isoelectric point (pI) distributes from 7.82 (IbJAZ1.4) to 9.83 (IbJAZ8.2). The IbJAZs are alkaline (pI > 7) and contain more than one phosphorylation site. Up to 86% of the IbJAZs contain more Ser phosphorylation sites than Thr or Tyr phosphorylation sites. Most of the IbJAZs are unstable, with an instability index of more than 43. The GRAVY scores of IbJAZs are less than 0, which indicates that they are hydrophilic proteins. Subcellular localization prediction assay showed that most of the IbJAZs were located in the cytoplasm, but also in microbody (IbJAZ3.2), mitochondrial (IbJAZ8.1 and IbJAZ10.2), and nucleus (IbJAZ9). The three-dimensional structural models of IbJAZs with homology higher than 20% were predicted and showed in Figures S1 and S2. The result showed that all IbJAZs have α-helices, and four IbJAZs (IbJAZ3.2, IbJAZ6.1, IbJAZ10.1, and IbJAZ10.2) have β-sheets.
All the JAZs were separately mapped on 15 chromosomes of I. batatas, I. trifida, and I. triloba, and dispersed on 8, 9, and 8 chromosomes (Figure 1). In I. batatas, three IbJAZs were detected on LG8 and LG9, two on LG13 and LG15, one on LG1, LG4, LG10, and LG11, whereas no gene was detected on LG2, LG3, LG5, LG6, LG7, LG12, and LG14 (Figure 1a). In I. trifida and I. triloba, except ItfJAZ9.2 was located on Chr03 only in I. trifida, the distribution of other JAZs was similar. Three JAZs were detected on Chr10 and Chr11; two on Chr02 and Chr06; and one on Chr01, Chr05, Chr08, and Chr13 (Figure 1b,c). The results indicated that the distribution of JAZs is different and disproportionate on chromosomes in sweet potato and its two diploid relatives.

2.2. Phylogenetic Relationship of JAZs in Sweet Potato and Its Two Diploid Relatives

To study the evolutionary relationship of JAZs in I. batatas, I. trifada, I. triloba, and Arabidopsis, we constructed a phylogenetic tree for 56 JAZs of these four species (i.e., 14 in I. batatas, 15 in I. trifida, 14 in I. triloba, and 13 in Arabidopsis) (Figure 2). All JAZs were unevenly distributed, and they were divided into five subgroups (Group I to V) according to the evolutionary distance. The specific distribution of JAZs was as follows (total: I. batatas, I. trifida, I. triloba, Arabidopsis): Group I (24: 6, 6, 6, 6), Group II (9: 2, 2, 2, 3), Group III (7: 2, 2, 2, 1), Group IV (11: 3, 3, 3, 2), and Group V (5: 1, 2, 1, 1) (Figure 2; Table S1). We named IbJAZs, ItfJAZs, and ItbJAZs based on their homology with homologs in Arabidopsis, and only AtJAZ1/3/4/6/8/9/10 from Arabidopsis have homologous protein in I. batatas, I. trifada, and I. triloba. These results indicated that the number and type of JAZs distributed in each subgroup in sweet potato were similar with its two diploid relatives but different with Arabidopsis.
Furthermore, a total of 93 JAZ proteins from seven plant species (i.e., 13 in Arabidopsis, 9 in Beta vulgaris, 13 in C. sinensis, 15 in rice, 14 in I. batatas, 15 in I. trifida, and 14 in I. triloba) were used for the phylogenetic analysis. They were divided naturally into 10 sub-groups (G1 to G10) (Figure S3). The JAZs in I. batatas, I. trifida and I. triloba were specifically distributed in G1 (3, 3, 3), G2 (3, 3, 3), G5 (3, 3, 3), G8 (1, 2, 1), G9 (2, 2, 2), and G10 (2, 2, 2) (Figure S3). However, the G7 group had the maximal number of BvJAZs, the G6 group had the maximal number of CsJAZs, and the G3 and G4 groups had the maximal number of OsJAZs (Figure S3). These results may indicate that sweet potato and its two diploid relatives had a distant evolutionary relationship with B. vulgaris, C. sinensis, and rice.

2.3. Conserved Motif and Exon-Intron Structure Analysis of JAZs in Sweet Potato and Its Two Diploid Relatives

The 43 JAZs from I. batatas, I. trifida, and I. triloba were subjected to conserved motif analysis using the MEME website, and the five most conserved motifs were identified (Figure 3a and Figure S4a). We found that JAZs in the same subgroup have similar conserved motifs, whereas there were differences in the types of motifs between each subgroup. For example, motifs 1 contained NT domains, and they specifically exist in Group I; motifs 2 and motifs 3 contained TIFY domains, motifs 4 contained Jas domains, and they were found in almost all JAZs; motifs 5 were uncertainly domains and mainly located to the N-terminal in Group IV (Figure 3a). The seqLogos of the five most conserved motifs generated using all JAZs sequences revealed that these motifs were conserved in sweet potato and its two diploid relatives (Figure S4a). Next, we focused on the multiple sequence alignment of JAZ proteins in I. batatas and Arabidopsis (Figure S4b). The TIFY domains had a conserved T(I/V)FYXG sequence, and the Jas domains had a conserved SLX2FLXKRKXRX5PY sequence. They were relatively conserved in I. batatas and Arabidopsis. In addition, we found that even though the JAZs are highly homologous in I. batatas, I. trifida and I. triloba, they may differ in the number and species of conserved domains, such as IbJAZ1.2 (contained motifs 1, 2, 3, 4, and 5) and ItfJAZ1.2 (contained motifs 1, 2, and 3) in Group I, IbJAZ8.1 (contained motifs 2 and 3) and ItfJAZ8.1 (contained motifs 2, 3, and 4) in Group II, IbJAZ10.1 (contained motifs 2, 3, and 4) and ItbJAZ10.1 (contained motifs 2 and 3) in Group III, and IbJAZ3.2 (contained motifs 2, 3, and 4) and ItfJAZ3.2 (contained motifs 2 and 3) in Group IV (Figure 3a).
To better understand the structural diversity among the JAZs, the exon–intron structures were analyzed (Figure 3b). The number of exons in the JAZs ranged from 2 to 8. In detail, JAZs of Group I contained 3 to 5 exons, JAZs of Group II contained 2 or 3 exons, JAZs of Group III contained 4 to 6 exons, JAZs of Group IV contained 2 to 8 exons, and JAZs of Group V contained six exons (Figure 3b). We also found that the exon–intron structures of some homologous JAZs might be different in I. batatas compared with that in I. trifida and I. triloba, such as IbJAZ1.2 (contained five exons) and ItfJAZ1.2 (contained four exons); in Group I, IbJAZ8.1 (contained three exons) and ItfJAZ8.1 (contained two exons); in Group II, IbJAZ10.1 (contained six exons) and ItbJAZ10.1 (contained four exons); in Group III, and IbJAZ3.2 (contained four exons) and ItfJAZ3.2 (contained two exons); and in Group IV(Figure 3b). The results show that the JAZ gene family may have undergone a lineage-specific differentiation event in the sweet potato genome.

2.4. Cis-Element Analysis in the Promoter of IbJAZs in Sweet Potato

Cis-elements present in the upstream of JAZs play important roles in the gene functions involved in plant development and stress responses. Therefore, we extracted 2000 bp upstream sequences of IbJAZs in I. batatas and performed the cis-element analysis. According to the prediction function, the elements were grouped into five broad categories: core/binding, development, light, hormone, abiotic/biotic elements (Figure 4). All 14 JAZs possessed a large number of core promoter elements and binding sites, such as TATA-box, CAAT-box, and AT-TATA-box. Light-responsive elements, such as BOX4, GT1-motif, G-box, were founded in most of IbJAZs.
Moreover, some development-related elements were found in IbJAZs (Figure 4). For example, motif I, which was related to the root growth, was found only in IbJAZ1.2; the CAT-box, which was associated with meristem formation and cell division, was found in IbJAZ1.2, IbJAZ1.3, IbJAZ3.1, and IbJAZ10.1. Besides, hormonal-responsive elements were abundant in IbJAZs (Figure 4), including ABA-responsive element ABRE, MeJA-responsive elements CGTCA-motif and TGACG-motif, SA-responsive element TCA, GA-responsive elements P-box and TATC-box, and IAA-responsive elements AuxRR-core and TGA-element. In addition, some abiotic-responsive elements (Figure 4), such as drought-responsive element DRE core, MYB and MYC, and low temperature-responsive element LTR, were found in most JAZs. These results suggested that IbJAZs were involved in the regulation of plant growth and development and abiotic stress adaption in sweet potato.

2.5. Protein Interaction Network of IbJAZs in Sweet Potato

To explore the potential regulatory network of IbJAZs, we constructed an IbJAZs interaction network based on Arabidopsis orthologous proteins (Figure 5). Protein interaction prediction indicated that IbJAZs could interact with each other. They also interacted with TIFY family proteins (i.e., PPD1, PPD2, ZIM, ZML1, ZML2, and TIFY8). In addition, IbJAZs could interact with numerous transcription factor families proteins, such as bHLH (i.e., bHLH3, bHLH13, and bHLH14), MYC (i.e., MYC2, MYC3, and MYC4), MYB (MYB21 and MYB24), and AP2 (i.e., TOE2), and some hormone synthesis and signaling related proteins, such as jasmonate biosynthesis-related protein lipoxygenase 2 (LOX2) and ethylene signaling related protein ethylene insensitive 3 (EIN3). These results indicated that IbJAZs might participate in the hormone regulation network through interacting with related transcription factors and functional proteins.

2.6. Expression Analysis of JAZs in Sweet Potato and Its Two Diploid Relatives

2.6.1. Expression Analysis in Various Tissues

To investigate the potential biological functions of IbJAZs in growth and development, the expression levels in six representative tissues (i.e., callus, petiole, leaf, fibrous root, tuberous root, and stem) of I. batatas were analyzed using real-time quantitative PCR (qRT-PCR) (Figure 6). Interestingly, different subgroups showed diversified expression patterns in six tissues. IbJAZs in Group I showed higher expression levels in all tissues than in other subgroups. Among all the IbJAZs, three IbJAZs (i.e., IbJAZ1.2, IbJAZ6.1, and IbJAZ6.2) were highly expressed, whereas two IbJAZs (i.e., IbJAZ8.2 and IbJAZ10.2) were low-expressed in all tissues. Nevertheless, some IbJAZ showed tissue-specific expression, e.g., IbJAZ8.1 was highly expressed in fibrous root, IbJAZ10.1 was highly expressed in leaf, IbJAZ3.2 was highly expressed in roots, IbJAZ9 was highly expressed in callus, but IbJAZ1.1 was lowly expressed in the tuberous root. These results indicated that IbJAZs might play different roles in the tissue development of sweet potato.
In addition, we used RNA-seq data of seven tissues (i.e., callus, flower, flower bud, leaf, root 1, root 2, and stem) to study the expression patterns of ItfJAZs and ItbJAZs in I. trifida and I. triloba [44] (Figure S5). ItfJAZs and ItbJAZs in Group I showed higher expression levels than other subgroups, which was consistent with that in I. batatats. In I. trifida, six ItfJAZs (i.e., ItfJAZ1.1, ItfJAZ1.3, ItfJAZ6.1, ItfJAZ6.2, ItfJAZ8.1, and ItfJAZ10.1) were highly expressed, whereas ItfJAZ3.2 was lowly expressed in all tissues. Besides, ItfJAZ1.2 and ItfJAZ1.4 were lowly expressed in flower and flower bud, three ItfJAZs (i.e., ItfJAZ3.1, ItfJAZ9.1, and ItfJAZ9.2) were lowly expressed in root, ItfJAZ4 was lowly expressed in root and stem, ItfJAZ8.2 was lowly expressed in callus, and ItfJAZ10.2 was highly expressed in leaf, root, and stem (Figure S5a). In I. triloba, eight ItbJAZs (i.e., ItbJAZ1.1, ItbJAZ1.3, ItbJAZ1.4, ItbJAZ4, ItbJAZ6.2, ItbJAZ8.1, ItbJAZ8.2, and ItbJAZ9) were highly expressed, but three ItbJAZs (i.e., ItbJAZ3.1, ItbJAZ3.2, and ItbJAZ10.1) were lowly expressed in all tissues. Besides, ItbJAZ1.2 was lowly expressed in flower, ItbJAZ6.1 was lowly expressed in leaf, and ItbJAZ10.2 was highly expressed in root (Figure S5b). These results suggested that each JAZ gene had a different tissue expression pattern and played different regulatory roles in the growth and development of sweet potato and its two diploid relatives.

2.6.2. Expression Analysis of Hormone Response

The JAZ family plays a crucial role in the hormone signal transduction and crosstalk of plants. Thus, it is necessary to investigate the expression of JAZs under various hormonal treatments. We performed qRT-PCR to evaluate the expression level of IbJAZs in response to the hormone, including ABA, GA, IAA, MeJA, and SA. Under ABA treatment, most of IbJAZs were repressed, but two IbJAZs (i.e., IbJAZ6.2 and IbJAZ10.1) were significantly induced (Figure 7a). Under GA treatment, more than half of IbJAZs were significantly induced, specifically IbJAZ6.2, IbJAZ10.1, and IbJAZ10.2 were up-regulated, but five IbJAZs (i.e., IbJAZ1.1, IbJAZ1.4, IbJAZ8.1, IbJAZ8.2, and IbJAZ9) were repressed at most of the time points (Figure 7b). Under IAA treatment, six IbJAZs (i.e., IbJAZ1.1, IbJAZ1.3, IbJAZ3.1, IbJAZ4, IbJAZ6.1, and IbJAZ8.1) were significantly induced, but four IbJAZs (i.e., IbJAZ1.2, IbJAZ1.4, IbJAZ3.2, and IbJAZ8.2) were repressed (Figure 7c). Under MeJA treatment, most of IbJAZs were up-regulated, specifically IbJAZ3.2, IbJAZ8.1, and IbJAZ8.2 were significantly induced by 49-, 41-, and 72-fold, but two IbJAZs (i.e., IbJAZ1.4 and IbJAZ4) were repressed (Figure 7d). Under SA treatment, six IbJAZs (i.e., IbJAZ1.1, IbJAZ1.3, IbJAZ3.2, IbJAZ8.1, IbJAZ8.2, and IbJAZ9) were significantly up-regulated, specifically IbJAZ8.1 was significantly induced by 76-fold at 0.5 h, but four IbJAZs (i.e., IbJAZ1.4, IbJAZ6.1, IbJAZ10.1, and IbJAZ10.2) were repressed (Figure 7e). Among these IbJAZs, IbJAZ1.4 was down-regulated in almost all the five hormone treatments, whereas other IbJAZs were induced by two or more hormones. These results indicated that IbJAZs were differentially expressed in response to various hormone induction and participated in the crosstalk between various hormones.
In addition, we analyzed the expression patterns of ItfJAZs and ItbJAZs using the RNA-seq data of I. trifida and I. triloba under ABA, GA, and IAA treatments [44]. In I. trifida, compared with hormone control, ItfJAZ1.2 was induced by ABA and IAA treatments, whereas ItfJAZ1.4 was repressed under all ABA, GA, and IAA treatments (Figure S6a). In I. triloba, compared with hormone control, ItbJAZ6.1 was induced by all ABA, GA, and IAA treatments (Figure S6b). Most other JAZs respond to at least one hormone treatment in I. trifida and I. triloba. Furthermore, compared to the expression patterns of IbJAZs in sweet potato (Figure 7), the homologous JAZs in I. trifida and I. triloba responded differently to ABA, GA, and IAA treatments, which indicated that JAZs were involved in different hormonal pathways between sweet potato and its two diploid relatives.

2.6.3. Expression Analysis under Abiotic Stresses

To explore the possible roles of IbJAZs in abiotic stress response, we analyzed the expression level of IbJAZs under polyethylene glycol (PEG), NaCl, H2O2, and 10/4 ℃ (day/night) treatments by qRT-PCR (Figure 8). Under PEG treatment, most of IbJAZs were significantly up-regulated with IbJAZ8.1 particularly induced by 106-fold at 0.5 h, but four IbJAZs (i.e., IbJAZ1.4, IbJAZ4, IbJAZ6.1, and IbJAZ9) were repressed (Figure 8a). Under NaCl treatment, some IbJAZs (e.g., IbJAZ1.1, IbJAZ1.2, IbJAZ1.3, IbJAZ1.4, IbJAZ8.2, IbJAZ9, and IbJAZ10.2) were significantly up-regulated with IbJAZ9 particularly induced by 44-fold at 6 h, but IbJAZ8.1 was repressed (Figure 8b). Under H2O2 treatment, some IbJAZs (e.g., IbJAZ1.4, IbJAZ6.1, IbJAZ8.1, and IbJAZ8.2) were significantly induced, whereas IbJAZ10.1 was repressed (Figure 8c). Under 10/4 ℃ (day/night) treatment, some IbJAZs (i.e., IbJAZ1.1, IbJAZ1.4, IbJAZ8.1, and IbJAZ10.2) were significantly up-regulated, specifically IbJAZ8.1 was induced by 152-fold at 12 h, whereas IbJAZ3.2 was significantly repressed (Figure 8d). Among these IbJAZs, several IbJAZs, such as IbJAZ1.2 and IbJAZ 10.2, were induced by all the four abiotic stress treatments in sweet potato.
Moreover, we analyzed the expression patterns of IbJAZs using the RNA-seq data of a drought-tolerant variety Xu55-2 under PEG treatment and the RNA-seq data of a salt-sensitive variety Lizixiang and a salt-tolerant line ND98 under NaCl treatment [45,46]. Consistent with qRT-PCR results (Figure 8), the expression of IbJAZ6.1 was also repressed in Xu55-2 under PEG treatment (Figure 9a), and the expression of some IbJAZs (e.g., IbJAZ1.3, IbJAZ1.4, and IbJAZ10.2) were induced in ND98 under NaCl treatment (Figure 9b). Excluding IbJAZ1.2 and IbJAZ10.2, expression patterns of other IbJAZs were similar in both Lizixiang and ND98 under NaCl treatment (Figure 9b). Taken together, these results indicated that IbJAZs were differentially expressed in response to various abiotic stresses in sweet potato.
In addition, we also analyzed the expression patterns of ItfJAZs and ItbJAZs using the RNA-seq data of I. trifida and I. triloba under mannitol, NaCl, and 10/4 °C (day/night) treatments [44]. In I. trifida, compared with control, ItfJAZ1.4 and ItfJAZ8.2 were induced by mannitol and 10/4 °C (day/night) treatments, and ItfJAZ9.2 was induced by NaCl treatment (Figure S7a). In I. triloba, compared with control, ItbJAZ1.2, ItbJAZ3.1, and ItbJAZ8.2 were induced, whereas ItbJAZ3.2 and ItbJAZ9 were repressed by mannitol, NaCl, and 10/4 °C (day/night) treatments (Figure S7b). Moreover, compared to the expression patterns of IbJAZs in sweet potato, the homologous JAZs in I. trifida and I. triloba responded differently to mannitol, NaCl, and 10/4 °C (day/night) treatments, which indicated that JAZs were involved in different abiotic stress responses between sweet potato and its two diploid relatives.

3. Discussion

JAZ repressors were universally reported to participate in plant growth and development, playing hub roles in hormonal crosstalk and responding to environmental stresses and biotic challenges [47]. However, the functional roles of JAZ family genes are still poorly understood in sweet potato. As the genetic background of cultivated sweet potato is complex, previous studies on the sweet potato gene families mainly focused on its most probable progenitor diploids I. trifida [48,49,50,51]. In fact, the plant morphology of cultivated hexaploid sweet potato differs greatly from that of its diploid relatives, especially since its diploid relatives cannot form tuberous roots [44]. In this study, we systematically identified JAZ family genes and analyzed and compared their characteristics based on the draft genome sequence of cultivated hexaploid sweet potato and its two diploid relatives. Genome-wild study of JAZs plays an important guiding role in the further study of their function and molecular breeding of sweet potato.

3.1. Evolution of the JAZ Gene Family in Sweet Potato and Its Two Diploid Relatives

In this study, a total of 43 JAZs were identified from sweet potato and its two diploid relatives. The number of JAZs identified in I. batatas (14) is the same as I. triloba (14) (Figure 1 and Figure 2; Table S1) but is one less than that in I. trifida (15). These numbers were also similar to that of other higher plants, such as Arabidopsis (13), rice (15), and wheat (14) [13,22,52]. This result indicated that the JAZ gene members in sweet potato are relatively conserved during the evolutionary process. Genomic alignment reveals the differentiation and evolution of chromosomes [53]. The chromosome localization and distribution of JAZs in each chromosome were different between I. batatas, I. trifida, and I. triloba (Figure 1). Based on the phylogenetic relationship, JAZs are divided into five subgroups (Group I to V), and only AtJAZ1/3/4/6/8/9/10 from Arabidopsis found homologous proteins in I. batatas, I. trifada, I. triloba. Except for Group V, the number of JAZs distributed in each subgroup was the same in Group I to IV among I. batatas, I. trifida and I. triloba. However, the number and type of JAZs distributed in each subgroup of sweet potato and its two diploid relatives were different from those of Arabidopsis and other plants (Figure 2 and Figure S3). These results showed that the JAZ gene family might have undergone a lineage-specific differentiation event in the terrestrial plant genome.
In plants, a small number of introns evolve more quickly to respond to environmental changes, whereas the introns usually act as buffer zones or mutation-resistant fragments that reduce adverse mutations and insertions. Moreover, introns also play essential roles in mRNA export, transcriptional coupling, alternative splicing, gene expression regulation, and other biological processes [54,55]. We found that the exon–intron structures of some homologous JAZs might be different in I. batatas compared with that in I. trifida and I. triloba, and the number of exons and introns of I. batatas was generally higher than that of I. trifida and I. triloba. For example, IbJAZ1.2 (contained five exons) and its homologous gene ItfJAZ1.2 (contained four exons) in Group I, IbJAZ8.1 (contained three exons) and its homologous gene ItfJAZ8.1 (contained two exons) in Group II, IbJAZ10.1 (contained six exons) and its homologous gene ItbJAZ10.1 (contained four exons) in Group III, and IbJAZ3.2 (contained four exons) and its homologous gene ItfJAZ3.2 (contained two exons) in Group IV (Figure 3). Therefore, homologous JAZs with more exon and introns in hexaploid sweet potato are evolutionally more complex than its two diploid relatives and thus participate in more precise growth and development and response to environmental stress.
In addition, the five most conserved motifs were identified from all 43 JAZs, and these motifs were highly conserved in sweet potato and its two diploid relatives (Figure 3a and Figure S4a). The same subgroup of JAZs usually has similar conserved motifs, whereas the types of motifs were generally different between each subgroup. The two core TIFY and Jas domains, which play irreplaceable roles in the JA signaling pathway, were present in almost all 43 JAZs from I. batatas, I. trifida, and I. triloba. While motif 1 specifically existed in Group I, and motif 5 was mainly located to the N-terminal in Group IV (Figure 3a). Therefore, JAZs with different motifs differentiated into a variety of biological functions during plant life activities in sweet potato.

3.2. Different Functions of JAZs on Growth and Development between Sweet Potato and Its Two Diploid Relatives

JAZ proteins play essential roles in plant growth and development. In Arabidopsis, AtCOI1-AtJAZ9 interaction mediated root growth inhibition [56,57]. AtJAZ7 and AtJAZ10 regulated leaf senescence through dark induction [58]. In rice, overexpression of OsJAZ13 activated hypersensitive cell death response and resulted in root attenuation [59]. In tomato, overexpression of SlJAZ2 led to leaf initiation, lateral bud emergence, and flowering transition [60]. Here, the cis-element prediction analysis showed that IbJAZ1.2 contained a root growth-related element motif I, and IbJAZ1.2, IbJAZ1.3, IbJAZ3.1, and IbJAZ10.1 contained meristem formation and cell division-related element CAT-box (Figure 4). To further explore the functions on growth and development of JAZs, we analyzed their expression level in the representative tissues of sweet potato and its two diploid relatives. The results indicated that JAZ family was differentially and constitutively expressed. The JAZs in Group I showed relatively high levels in all tissues compared to other subgroups of I. batatas, I. trifida and I. triloba (Figure 6 and Figure S5). IbJAZ1.2, which contained a motif I and a CAT-box, was highly expressed in fibrous and tuberous root, but ItfJAZ1.2 and ItbJAZ1.2 were expressed most highly in the stem and root, indicating that IbJAZ1.2 might play regulatory roles in tuberous root development of sweet potato. Moreover, IbJAZ10.1, which contained a CAT-box, was only highly expressed in leaf, but ItfJAZ10.1 and ItbJAZ10.1 were most highly expressed in the stem, indicating that IbJAZ10.1 might be involved in leaf development in sweet potato. The plant morphology of cultivated hexaploid sweet potato differs greatly from that of its diploid relatives, especially since its diploid relatives cannot form tuberous roots [44]. Different tissue expression patterns of homologous JAZ genes may contribute to tissue diversification in sweet potato and its two diploid relatives.

3.3. Different Functions of JAZs on Hormone Crosstalk between Sweet Potato and Its Two Diploid Relatives

Multiple interacting hormone pathways play a major role in many biological processes, including plant growth, development, and defense against a wide range of both biotic and abiotic stresses [6]. In Arabidopsis, JAZ9 inhibited the interaction of RGA (a DELLA protein) with the transcription factor PIF3 and formed a COI1-JAZ-DELLA-PIF signaling module to regulate plant defense and growth by interfering with JA and GA signaling cascade [61]. AtERF109 activity was inhibited by direct interaction with JAZ proteins to prevent hypersensitivity to wounding, which led to JA and IAA signaling crosstalk [62]. In wheat, TaJAZ1 interacted with TaABI5 to connect the signaling between JA and ABA and modulate seed germination [63]. In grape, VqJAZ4 enhanced disease defense responses through JA and SA signaling pathways [64]. In this study, protein interaction prediction showed that IbJAZs could interact with each other and also interacted with some hormone synthesis and signaling related proteins to participate in multiple hormone pathways, including TIFY family proteins PPD1, PPD2, ZIM, ZML1, ZML2, and TIFY8, jasmonate biosynthesis-related protein LOX2, and ethylene signaling related protein EIN3 (Figure 5). In addition, most of IbJAZs were induced by two or more hormones (Figure 7). IbJAZ1.3 and IbJAZ3.2, which contained JA-responsive elements CGTCA-motif and TGACG-motif, were induced by GA, MeJA, and SA treatment, whereas ItbJAZ3.2 was induced by IAA treatment. IbJAZ4 and IbJAZ6.1, which contained IAA-responsive element TGA, were significantly induced under GA and IAA treatments, whereas ItbJAZ6.1 was induced under ABA, GA, and IAA treatments. IbJAZ6.2, which contained ABA-responsive element ABRE, GA-responsive element P-box, and JA-responsive elements CGTCA-motif and TGACG-motif, was highly induced by ABA, GA, and MeJA, whereas ItfJAZ6.2 and ItbJAZ6.2 showed no significant change. IbJAZ8.2 and IbJAZ9, which contained an SA-responsive element TCA-element, were highly expressed under MeJA and SA treatments, whereas ItbJAZ8.2 was highly expressed under ABA treatment. IbJAZ10.1, which contained ABA-responsive element ABRE and JA-responsive elements CGTCA-motif and TGACG-motif, was significantly induced by ABA and MeJA treatment, whereas ItbJAZ10.1 was induced by GA treatment. These results indicated that JAZs participated in multiple hormones crosstalk, and homologous JAZ genes were involved in different hormonal pathways in sweet potato and its two diploid relatives.

3.4. Different Functions of JAZs on Abiotic Stress Response between Sweet Potato and Its Two Diploid Relatives

JAZ proteins directly interact with or repress many TFs to modulate abiotic stress tolerance efficiently. In cotton, GbWRKY1 could function as a negative regulator of ABA signaling via JAZ1 and ABI1, with effects on salt and drought tolerance [65]. In soybean, GmWRKY40 interacted with eight JAZ proteins and regulated reactive oxygen species accumulation [31]. In banana, MaJAZ1 attenuated the transcriptional activation of MaAOC2 and modulated cold tolerance [66]. In apple, MdbHLH1 interacted with MdJAZ1/4 and MdMYC2, which could bind to the MdCBF1 promoter, to enhance cold tolerance [67]. Here, protein interaction prediction showed that IbJAZs could interact with numerous transcription factors, such as bHLH3/13/14, MYC2/3/4, MYB21/24, and TOE2 [68], to participate in growth and development and biotic and abiotic stresses in sweet potato.
In addition, IbJAZs significantly responded to various abiotic stresses in sweet potato (Figure 8 and Figure 9). IbJAZ3.1, containing drought-responsive element MYC, was highly induced by PEG treatment at most of the time points; IbJAZ1.1, IbJAZ1.3, IbJAZ1.4, IbJAZ9, and IbJAZ10.2 were highly induced by NaCl treatment; IbJAZ1.4, IbJAZ6.1, IbJAZ8.1, and IbJAZ8.2 were highly induced by H2O2 treatment; and IbJAZ1.1 containing a cold-responsive element LTR, IbJAZ1.4, IbJAZ8.1, and IbJAZ10.2 were highly induced by 10/4 ℃ (day/night) treatment, suggesting that they might be involved in drought, salt, oxidation, and cold tolerance of sweet potato, respectively (Figure 8).
The results from the qRT-PCR and RNA-seq data analysis of sweet potato and its two diploid relatives under abiotic stress indicated that homologous JAZs in I. trifida and I. triloba responded differently compared to that of sweet potato (Figure S7). This means that JAZs were involved in different abiotic stress responses between sweet potato and its two diploid relatives. The diploid I. trifida and I. triloba could be used to discover functional genes, particularly genes conferring resistance or tolerance to biotic and abiotic stresses, which had been possibly lost in the cultivated sweet potato during its domestication [69]. In this study, 15 ItfJAZs were identified in I. trifida, which was one more (ItfJAZ9.2) than that in sweet potato. ItfJAZ9.2 was induced by NaCl treatment. Furthermore, ItfJAZ1.4 and ItfJAZ8.2 were induced by mannitol and 10/4 °C (day/night) treatments (Figure S7a). ItbJAZ1.2, ItbJAZ3.1, and ItbJAZ8.2 were induced by all mannitol, NaCl, and 10/4 °C (day/night) treatments (Figure S7b). These JAZs may serve as candidate genes for use in improving abiotic stress tolerance in sweet potato.

4. Materials and Methods

4.1. Identification of JAZs

The whole genome sequences of I. batatas, I. trifida, and I. triloba were downloaded from Ipomoea Genome Hub (https://ipomoea-genome.org/, accessed on 15 March 2021) and Sweetpotato Genomics Resource (http://sweetpotato.plantbiology.msu.edu/, accessed on 15 March 2021). To accurately identify all JAZs family members, three different screening methods were combined. Firstly, the BLAST algorithm was used to identify predicted JAZs using all AtJAZs from the Arabidopsis genome database (https://www.arabidopsis.org/, accessed on 15 March 2021) as queries (BLASTP, E value ≤ 1 × 10−5). Next, the HMMER 3.0 software (Harvard University, Cambridge, MA, USA) was used to identify potential JAZs through the Hidden Markov Model profiles (hmmsearch, E value ≤ 1 × 10−5) of the TIFY domain (PF06200) and Jas domain (PF09425), which were extracted from the Pfam databases (http://pfam.xfam.org/, accessed on 15 March 2021). Finally, all putative JAZs were ensured using SMART (http://smart.embl-heidelberg.de/, accessed on 16 March 2021) and CD-search (https://www.ncbi.nlm.nih.gov/Structure/cdd/wrpsb.cgi, accessed on 16 March 2021).

4.2. Chromosomal Distribution of JAZs

The IbJAZs, ItfJAZs, and ItlJAZs were separately mapped to the I. batatas, I. trifida, and I. triloba chromosome based on the chromosomal location provided in the Ipomoea Genome Hub (https://ipomoea-genome.org/, accessed on 15 March 2021) and Sweetpotato Genomics Resource (http://sweetpotato.plantbiology.msu.edu/, accessed on 15 March 2021). The visualization was generated by the TBtools software (South China Agricultural University, Guangzhou, China).

4.3. Protein Properties Prediction of JAZs

The MW, theoretical pI, unstable index, hydrophilic of JAZs were calculated by ExPASy (https://www.expasy.org/, accessed on 20 March 2021). The phosphorylation sites of JAZs were predicted using Kinase Phos (http://kinasephos.mbc.nctu.edu.tw/, accessed on 20 March 2021). The subcellular localization of JAZs was predicted by PSORT (https://wolfpsort.hgc.jp/, accessed on 20 March 2021). The 3D structural model of JAZs was built using SWISS-MODEL (https://swissmodel.expasy.org/, accessed on 20 March 2021) [70].

4.4. Phylogenetic Analysis of JAZs

The phylogenetic analysis of JAZs from Arabidopsis, Beta vulgaris, C. sinensis, rice, I. batatas, I. trifida, and I. triloba was performed using ClustalW in MEGA 7.0 (Temple University, Philadelphia, USA) [71] with default parameters, maximum likelihood method, and Poisson correction model were used. The bootstrap was performed with 1000 replicates. Then, the phylogenetic tree was constructed by iTOL (http://itol.embl.de/, accessed on 1 September 2021). The protein sequences were downloaded from the National Center for Biotechnology Information (https://www.ncbi.nlm.nih.gov/, accessed on 31 August 2021).

4.5. Domain Identification and Conserved Motifs Analysis of JAZs

The conserved motifs of JAZs were analyzed by MEME (https://meme-suite.org/meme/, accessed on 18 March 2021), the maximum number of motifs parameter was set to 5. The multiple sequence alignment of the TIFY and Jas domains was built using the DNAMAN software (lynnonBiosoft, San Ramon, CA, USA).

4.6. Exon–Intron Structures and Promoter Analysis of JAZs

The exon–intron structures of JAZs were obtained by GSDS 2.0 (Peking University, Beijing, China) (http://gsds.gao-lab.org/, accessed on 19 March 2021) and were visualized by the TBtools software (South China Agricultural University, Guangzhou, China). The cis-elements in the approximately 2000 bp promoter region of JAZs were predicted by PlantCARE (http://bioinformatics.psb.ugent.be/webtools/plantcare/html/, accessed on 21 March 2021) [72].

4.7. Protein Interaction Network of JAZs

The protein interaction network of JAZs was predicted by GeneMAINA (http://genemania.org/, accessed on 31 August 2021) and String (https://www.string-db.org/, medium confidence 0.400, accessed on 31 August 2021) based on Arabidopsis orthologous proteins. The network map was built by Cytoscape software 3.2 (Institute for Systems Biology, Seattle, WA, USA) [73].

4.8. qRT-PCR Analysis of JAZs

The salt-tolerant sweet potato (I. batatas) line ‘ND98′ was used for qRT-PCR analysis in this study [46]. In vitro-grown ND98 plants were cultured on Murashige and Skoog (MS) medium at 27 ± 1 °C under a photoperiod consisting of 13 h of cool-white fluorescent light at 54 μmol m–2 s–1 and 11 h of darkness. Sweet potato plants were cultivated in a field at the campus of China Agricultural University, Beijing, China.
For expression analysis in various tissues, total RNA was extracted from the fibrous root, tuberous root, stems, leaves, petioles, and bud tissues of 3-month-old field-grown ND98 plants using the TRIzol method (Invitrogen, Carlsbad, CA, USA). For expression analysis of hormone and abiotic treatment, the leaves were sampled at 0, 0.5, 1, 3, 6, 12, 24, and 48 h after treated with 200 mM NaCl, 20% PEG6000, 10 mM H2O2, 10/4 ℃ (day/night), 100 μM ABA, 100 μM GA, 100 μM MeJA, 100 μM SA, and 100 μM IAA, respectively. Three independent biological replicates were taken, each with three plants. qRT-PCR was conducted using the SYBR detection protocol (TaKaRa, Kyoto, Japan) on a 7500 Real-Time PCR system (Applied Biosystems, Foster City, CA, USA). The reaction mixture was composed of first-strand cDNA, primer mix, and SYBR Green M Mix (TaKaRa; code RR420A) to a final volume of 20 μL. A sweet potato actin gene (GenBank AY905538, 20, 5, 21) was used as an internal control. The relative gene expression levels were quantified with the comparative CT method [74]. The specific primers of qRT-PCR analysis were listed in Table S2. The heat maps of gene expression profiles were constructed using TBtools software.

4.9. Transcriptome Analysis

The RNA-seq data of ItfJAZs and ItlJAZs in I. trifida and I. triloba were downloaded from the Sweetpotato Genomics Resource (http://sweetpotato.plantbiology.msu.edu/, accessed on 12 April 2021). The RNA-seq data of IbJAZs in I. batatas were obtained from related research in our laboratory [45,46]. The expression levels of JAZs were calculated as fragments per kilobase of exon per million fragments mapped (FPKM). The heat maps were constructed by TBtools software.

5. Conclusions

In this study, we identified and characterized 43 JAZs in cultivated hexaploid sweet potato (I. batatas, 2n = 6x = 90, 14), and its two diploid relatives I. trifida (2n = 2x = 30, 15) and I. triloba (2n = 2x = 30, 14) based on genome and transcriptome data. The protein physiological properties, chromosome localization, phylogenetic relationship, gene structure, promoter cis-elements, and protein interaction network of these 43 JAZs were systematically investigated. Moreover, the tissue specificity and expression pattern analysis for hormone response and abiotic stress of JAZs were analyzed by qRT-PCR and RNA-seq. Our results indicated that there was a differentiation in roles played by homologous JAZs, and each JAZ gene played different vital roles in growth and development, hormone crosstalk, and abiotic stress response between sweet potato and its two diploid relatives. This work provided valuable insights into the structure and function of JAZ genes in sweet potato and its two diploid relatives.

Supplementary Materials

The following are available online at https://www.mdpi.com/article/10.3390/ijms22189786/s1.

Author Contributions

H.Z. (Huan Zhang) and S.H. conceived and designed the research. Z.H., Z.W., X.L. and N.Z. performed the experiments. Z.W., Z.H. and S.G. analyzed the data. H.Z. (Huan Zhang) and Z.W. wrote the paper. Q.L. and H.Z. (Hong Zhai) revised the paper. All authors have read and agreed to the published version of the manuscript.

Funding

This work was funded by grants from the Beijing Natural Science Foundation (grant no. 6212017), the National Key R&D Program of China (2019YFD1001301/2019YFD1001300), the National Natural Science Foundation of China (grant no. 31901584), the National Natural Science Foundation of China (grant no. 31771856), China Agriculture Research System of MOF and MARA (CARS-10, Sweetpotato), the Beijing Food Crops Innovation Consortium Program (BAIC09-2021), and the Chinese Universities Scientific Fund (2020TC085).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study are available on request from thecorresponding author.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Chromosomal localization and distribution of JAZ genes in I. batatas (a), I. trifida (b), and I. triloba (c). The bars represent chromosomes, the chromosome numbers are displayed on the left side, and the gene names are displayed on the right side. The relative chromosomal localization of each JAZ gene is marked on the black line of the right side and indicated by the unit Mbp. Details chromosomal location information is listed in Table S1.
Figure 1. Chromosomal localization and distribution of JAZ genes in I. batatas (a), I. trifida (b), and I. triloba (c). The bars represent chromosomes, the chromosome numbers are displayed on the left side, and the gene names are displayed on the right side. The relative chromosomal localization of each JAZ gene is marked on the black line of the right side and indicated by the unit Mbp. Details chromosomal location information is listed in Table S1.
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Figure 2. Phylogenetic analysis of the JAZ family in I. batatas, I. trifida, I. triloba, and Arabidopsis. A total of 56 JAZs were divided into five subgroups (Group I to V) according to the evolutionary distance. The red circles represent the 14 IbJAZs in I. batatas. The green squares represent the 15 ItfJAZs in I. trifida. The yellow squares represent the 14 ItbJAZs in I. triloba. The blue letters represent the 13 AtJAZs in Arabidopsis.
Figure 2. Phylogenetic analysis of the JAZ family in I. batatas, I. trifida, I. triloba, and Arabidopsis. A total of 56 JAZs were divided into five subgroups (Group I to V) according to the evolutionary distance. The red circles represent the 14 IbJAZs in I. batatas. The green squares represent the 15 ItfJAZs in I. trifida. The yellow squares represent the 14 ItbJAZs in I. triloba. The blue letters represent the 13 AtJAZs in Arabidopsis.
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Figure 3. Conserved motifs and exon–intron structure analysis of JAZ family in I. batatas, I. trifida, and I. triloba. (a) The phylogenetic tree showed that JAZs were distributed to five subgroups in the left, and the five conserved motifs were shown in different colors. The red squares represent the IbJAZs. (b) Exon–intron structures of JAZs. The purple boxes, yellow boxes, and black lines represent the UTRs, exons, and introns, respectively.
Figure 3. Conserved motifs and exon–intron structure analysis of JAZ family in I. batatas, I. trifida, and I. triloba. (a) The phylogenetic tree showed that JAZs were distributed to five subgroups in the left, and the five conserved motifs were shown in different colors. The red squares represent the IbJAZs. (b) Exon–intron structures of JAZs. The purple boxes, yellow boxes, and black lines represent the UTRs, exons, and introns, respectively.
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Figure 4. Cis-elements analysis of IbJAZs in I. batatas. The cis-elements were divided into five broad categories. The degree of red colors represents the number of cis-elements upstream of the IbJAZs.
Figure 4. Cis-elements analysis of IbJAZs in I. batatas. The cis-elements were divided into five broad categories. The degree of red colors represents the number of cis-elements upstream of the IbJAZs.
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Figure 5. Functional interaction networks of IbJAZ in I. batatas according to orthologues in Arabidopsis. Network nodes represent proteins, and lines represent protein–protein associations. The red dotted lines represent the strong interactions of JAZs with each other. The gray lines represent physical interactions. The blue lines represent shared protein domains. The orange lines represent co-expression. The purple lines represent co-localization. The line thickness represents the strength of the interaction.
Figure 5. Functional interaction networks of IbJAZ in I. batatas according to orthologues in Arabidopsis. Network nodes represent proteins, and lines represent protein–protein associations. The red dotted lines represent the strong interactions of JAZs with each other. The gray lines represent physical interactions. The blue lines represent shared protein domains. The orange lines represent co-expression. The purple lines represent co-localization. The line thickness represents the strength of the interaction.
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Figure 6. Gene expression patterns of IbJAZs in different tissues (callus, petiole, leaf, fibrous root, tuberous root, and stem) of I. batatas. The values were determined by RT-qPCR from three biological replicates consisting of pools of three plants, and the results were analyzed using the comparative CT method. The expression of IbJAZ10.1 in fibrous root was considered as “1”. Fold change ± SD was shown in the boxes. Different lowercase letters indicate a significant difference of each IbJAZ at p < 0.05 based on Student’s t-test.
Figure 6. Gene expression patterns of IbJAZs in different tissues (callus, petiole, leaf, fibrous root, tuberous root, and stem) of I. batatas. The values were determined by RT-qPCR from three biological replicates consisting of pools of three plants, and the results were analyzed using the comparative CT method. The expression of IbJAZ10.1 in fibrous root was considered as “1”. Fold change ± SD was shown in the boxes. Different lowercase letters indicate a significant difference of each IbJAZ at p < 0.05 based on Student’s t-test.
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Figure 7. Gene expression patterns of IbJAZs in response to different phytohormone, i.e. (a) ABA, (b) GA, (c) IAA, (d) MeJA, and (e) SA of I. batatas. The values were determined by RT-qPCR from three biological replicates consisting of pools of three plants, and the results were analyzed using the comparative CT method. The expression of 0 h in each treatment was considered as “1”. The fold change ± SD was shown in the boxes. Different lowercase letters indicate a significant difference of each IbJAZ at p < 0.05 based on Student’s t-test.
Figure 7. Gene expression patterns of IbJAZs in response to different phytohormone, i.e. (a) ABA, (b) GA, (c) IAA, (d) MeJA, and (e) SA of I. batatas. The values were determined by RT-qPCR from three biological replicates consisting of pools of three plants, and the results were analyzed using the comparative CT method. The expression of 0 h in each treatment was considered as “1”. The fold change ± SD was shown in the boxes. Different lowercase letters indicate a significant difference of each IbJAZ at p < 0.05 based on Student’s t-test.
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Figure 8. Gene expression patterns of IbJAZs in response to abiotic stresses, i.e. (a) PEG, (b) NaCl, (c) H2O2, and (d) 10/4 °C treatments of I. batatas. The values were determined by RT-qPCR from three biological replicates consisting of pools of three plants, and the results were analyzed using the comparative CT method. The expression of 0 h in each treatment was considered as “1”. The fold change ± SD was shown in the boxes. Different lowercase letters indicate a significant difference of each IbJAZ at p < 0.05 based on Student’s t-test.
Figure 8. Gene expression patterns of IbJAZs in response to abiotic stresses, i.e. (a) PEG, (b) NaCl, (c) H2O2, and (d) 10/4 °C treatments of I. batatas. The values were determined by RT-qPCR from three biological replicates consisting of pools of three plants, and the results were analyzed using the comparative CT method. The expression of 0 h in each treatment was considered as “1”. The fold change ± SD was shown in the boxes. Different lowercase letters indicate a significant difference of each IbJAZ at p < 0.05 based on Student’s t-test.
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Figure 9. Gene expression patterns of IbJAZs under PEG and NaCl treatments as determined by RNA-seq. (a) Expression analysis of IbJAZs under PEG treatment in a drought-tolerant variety Xu55-2. (b) Expression analysis of IbJAZs under NaCl treatment in a salt-sensitive variety Lizixiang and a salt-tolerant line ND98. Log2 (FPKM ± SD) was shown in the boxes. Different lowercase letters indicate a significant difference of each IbJAZ at p < 0.05 based on Student’s t-test.
Figure 9. Gene expression patterns of IbJAZs under PEG and NaCl treatments as determined by RNA-seq. (a) Expression analysis of IbJAZs under PEG treatment in a drought-tolerant variety Xu55-2. (b) Expression analysis of IbJAZs under NaCl treatment in a salt-sensitive variety Lizixiang and a salt-tolerant line ND98. Log2 (FPKM ± SD) was shown in the boxes. Different lowercase letters indicate a significant difference of each IbJAZ at p < 0.05 based on Student’s t-test.
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Table
Table 1. Characterization of IbJAZs in sweet potato.
Table 1. Characterization of IbJAZs in sweet potato.
Gene IDGene NameCDS (bp)Protein (aa)Genomic (bp)MW (kDa)pIPhosphorylation SiteInstabilityGravySubcellular
SerThrTyr
Ib13g55036IbJAZ1.11175249199026.7309.5611043.47−0.549cytoplasm
Ib15g60879IbJAZ1.21334228181225.1129.7340052.26−0.553cytoplasm
Ib08g31186IbJAZ1.31728210263323.1108.8141147.07−0.469cytoplasm
Ib13g55166IbJAZ1.41069261241127.9457.8250049.55−0.634cytoplasm
Ib08g31615IbJAZ3.114922703663281.339.7230058.99−0.047cytoplasm
Ib11g46572IbJAZ3.27591611629177.199.1040048.82−0.074microbody
Ib09g35530IbJAZ42118384405040.7439.5263052.80−0.069cytoplasm
Ib15g60960IbJAZ6.1847210119322.6878.7641049.85−0.587cytoplasm
Ib08g31288IbJAZ6.21400268216430.2688.8570054.40−0.605cytoplasm
Ib09g34766IbJAZ8.1778151122917.0078.6250080.04−0.340mitochondrial
Ib09g37258IbJAZ8.263713891815.5859.8320078.45−0.430cytoplasm
Ib01g540IbJAZ910742242162246.599.1022164.44−0.448nucleus
Ib04g13640IbJAZ10.1837189316320.7188.8640066.19−0.372cytoplasm
Ib10g39764IbJAZ10.21317178372819.3569.3960069.18−0.299mitochondrial
CDS, coding sequence; MW, molecular weight; pI, isoelectric point; Ser, serine; Thr, threonine; Tyr, tyrosine.
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Huang, Z.; Wang, Z.; Li, X.; He, S.; Liu, Q.; Zhai, H.; Zhao, N.; Gao, S.; Zhang, H. Genome-Wide Identification and Expression Analysis of JAZ Family Involved in Hormone and Abiotic Stress in Sweet Potato and Its Two Diploid Relatives. Int. J. Mol. Sci. 2021, 22, 9786. https://doi.org/10.3390/ijms22189786

AMA Style

Huang Z, Wang Z, Li X, He S, Liu Q, Zhai H, Zhao N, Gao S, Zhang H. Genome-Wide Identification and Expression Analysis of JAZ Family Involved in Hormone and Abiotic Stress in Sweet Potato and Its Two Diploid Relatives. International Journal of Molecular Sciences. 2021; 22(18):9786. https://doi.org/10.3390/ijms22189786

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Huang, Zhengwei, Zhen Wang, Xu Li, Shaozhen He, Qingchang Liu, Hong Zhai, Ning Zhao, Shaopei Gao, and Huan Zhang. 2021. "Genome-Wide Identification and Expression Analysis of JAZ Family Involved in Hormone and Abiotic Stress in Sweet Potato and Its Two Diploid Relatives" International Journal of Molecular Sciences 22, no. 18: 9786. https://doi.org/10.3390/ijms22189786

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