Open Access
Review

Advances in the regulation of plant development and stress response by miR167

Xia Liu1,2,†,Sheng Huang1,2,†,Hongtao Xie2,*
1
Shandong Provincial Key Laboratory of Plant Stress Research, College of Life Science, Shandong Normal University, 250014 Jinan, Shandong, China
2
Bellagen Biotechnology Co., Ltd., 250000 Jinan, Shandong, China
DOI: 10.52586/4974 Volume 26 Issue 9, pp.655-665
Submited: 26 May 2021 Revised: 13 July 2021
Accepted: 28 July 2021 Published: 30 September 2021
*Corresponding Author(s):  
Hongtao Xie
E-mail:  
xiehongtao@bellagen.cn
These authors contributed equally.
Copyright: © 2021 The author(s). Published by BRI. This is an open access article under the CC BY 4.0 license (https://creativecommons.org/licenses/by/4.0/).
Abstract

MicroRNAs (miRNAs) are a class of endogenous, non-coding small RNA that cleavage mRNA targets in sequence-specific manner or the inhibition of translation, which regulates gene expression at the post-transcriptional level. miRNAs are involved in the regulation of plant growth, metabolism and stress response. miR167 family is one of the highly conserved miRNA families in plants. It functions mainly by regulating the auxin response factors (ARFs) and IAA-Ala resistant3 (IAR3) genes, and participates in regulating the development of roots, stems, leaves and flowers, flowering time, embryonic development, seed development and stress response. Here, we reviewed the biological functions of miR167 family and its target genes in plant growth and development and stress response, and further discussed the application prospect of miR167 in agricultural production. Furthermore, this review provides references for the further study of miR167 family in plants.

Key words

miR167; Target gene; Biological function; Stress; Agricultural production

2. Introduction

MicroRNAs (miRNAs) are small endogenous noncoding RNAs with a length of 20–24 nucleotides. Plant miRNA genes (MIRs) are transcribed by RNA polymerase II into a primary transcript with stem-loop structure, after a series of cutting processes, mature miRNAs are formed [1, 2, 3]. It can regulate the target gene expression by cleaving or inhibiting the translation of mRNA [4, 5]. miRNAs play an active role in basic physiological and morphological processes and response to various stresses in plants.

MicroRNA167 (miR167) is widely distributed in plants and plays an active role in regulating plant growth and development. According to recent studies, miR167 is involved in the regulation of plant vegetative and reproductive organ development, flowering time and stress response through the regulation of its major target genes such as ARF6, ARF8 and IAR3. In addition, miR167 targets ARF12, ARF17, ARF25, ubiquitin-protein ligase AIRP2 and natural resistance-associated macrophage proteins (NRAMPs) genes is involved in the regulation of plant growth and development. In this paper, the biological functions of miR167 and its target gene in plant growth and stress response were reviewed, the regulation mechanism of miR167 in plant growth and development was discussed, and the application prospect of miR167 in agricultural production was prospected. The research progress of miR167 in recent years is detailed in Table 1 (Ref. [6, 7, 8, 9, 10, 11, 12, 13, 14, 15, 16, 17, 18, 19, 20, 21, 22]).

Table 1: Research progress of miR167 in recent years.
miRNA Target gene Function References
miR167a AtARF6/AtARF8 Promote lateral root growth and increase in number [6, 7]
miR167c GmARF8a/GmARF8b Lateral root growth and nodule development [8]
miR167b OsARF6/OsARF12/OsARF17/OsARF25 Reduced plant height and tiller number [9]
miR167a SpARF6/SpARF8 Internodes, leaf blade reduced/petals, stamens, and style shortened [10]
miR167 NtARF6/NtARF8 Leaf blade curled and wrinkled/flowering [11]
miR167a/miR167b/miR167c AtARF6/AtARF8 Ovules develop/filaments shorten/anthers elongate and do not dehisce/seeds develop/somatic embryogenesis/stomata open [12, 13, 14, 15, 16]
miR167 InARF8 Development of shoot apices, leaf primordia and pistil organs/regulated stomatal opening [17]
miR167a CsARF8 Seed size and delayed seed maturity [18]
miR167 TcARF6 Response to salt stress [19]
miR167d OSARF12 Protection against germs [20]
miR167a IAR3 Resistance to pathogen/osmotic stress [21]
miR167 Regulating stomata opening [22]

3. miR167 family and its target gene

3.1 miR167 family

miR167 is one of the highly conserved gene family in plants. It has different stem-loop precursors and produce mature miR167 sequences. In the miR167 sequence, processing from 3’end is significantly different from that from 5’end, and primary miR167 and mature miR167 have different expression patterns in plants [23, 24, 25].

The miR167 family is found mainly in angiosperms, is more widespread in dicotyledones than in monocots, and has been identified in soybean (Glycine max), peanut (Arachis hypogaea), apple, corn (Zea mays), wheat, longan (Dimocarpus longan Lour) and sugarcane, etc. The number of miR167 precursors and mature bodies varied among different species, the number of miR167 precursors varied from 1 to 12, and the number of mature bodies varied from 1 to 22 [26]. miR167 is species-specific, such as in Arabidopsis thaliana, four miR167 genes (MIR167a, MIR167b, MIR167c and MIR167d), miR167a produces higher levels of miR167 maturation, and miR167a is the main miR167 gene family member that regulates the development of female and male organs [15, 27]. miR167 family of rice (Oryza sativa) is encoded by 10 loci, miR167a–j, there is only one nucleotide difference in the 30-end between miR167a–c and miR167d–j. Among these ten genes, MIR167a, MIR167b and MIR167c can produce mature miR167 more efficiently, and miR167a–c plays a major role in rice, affecting plant size and tiller number [9]. In soybean (Glycine max), miR167 family has 11 highly conserved homologous miRNAs, which can be divided into two subgroups include miR167a/b/d/e/f/g/h/i/j/k and miR167c. miR167 primary transcripts are produced by different genes, mature miR167 had only one or two nucleotide differences at the 3’end or 5’end, and miR167 mediated nodulation in soybean [8].

3.2 miR167 target gene

miR167 can target different target genes to participate in the regulation of plant growth and development, and miR167 cleavage of target genes seems to be a common way of post-transcriptional regulation. Auxin response factor (ARF) is a transcription factor that regulates the expression of auxin response genes. It can be combined with auxin response element (AUXRE) “TGTTC” in the promoter region of auxin response gene, auxin response genes are activated or inhibited and interact with the second transcription factor family, AUX/IAA repressor protein, to induce auxin response [28, 29, 30]. ARF transcription factors contain three domains: (1) a conserved B3 family of N-terminal DNA binding domain (DBD), and (2) a non-conserved middle region, which can activate or inhibit gene expression, (3) a conservative C-terminal domain (CTD) [31]. The C-terminal domain of ARF is similar to the III and IV domains of AUX IAA protein [32]. ARF and auxin (AUX) indole-3-acetic acid (IAA) can form dimers through this domain [33]. The number of ARF family members varies from species to species, such as there are 23 and 25 ARF family members in Arabidopsis thaliana [34] and in rice [35]. ARF gene was also identified in tomato (Solanum lycopersicum) [36], corn [37], rape (Brassica rapa) [38], soybean [39] and cassava (Manihot esculenta) [40, 41], etc. Auxin plays an important role in the whole life process from embryogenesis to senescence, and its function is mainly mediated by ARF and AUX/IAA [42, 43]. miR167 targets AtARF6 or AtARF8 to regulate the normal development of anthers and ovules, and AtARF6 and AtARF8 are cut at the complementary site of miR167 [27]. Auxin response factors ARF6 and ARF8 play a conservative role in the development of vegetative and reproductive organs, regulating the development of roots and stems, the elongation of stamen filaments, the dehiscence of anthers, the maturation of gynoecium and the flowering time [10, 44, 45]. ARF8 an ARF gene affected by environmental conditions. Light signal molecules strongly induce ARF8 gene expression in hypocotyl, but ARF8 is not induced in darkness [46]. Due to the functional conservativeness of ARF gene, it remains to be further studied that ARF6 and ARF8 are mediated by miR167 in the various processes of plant growth. In addition, OsARF6, OsARF12, OsARF17, OsARF25 genes and miR167 exhibited high sequence complementarity in almost the same manner. The 5’RACE technology proved that four OsARFs transcripts are cleaved by miR167, confirming that OsARF12, OsARF17 and OsARF25 are the target genes of miR167 in rice [9]. OsARF12 and ARF8 have high homology, and found that the 2467-2494 region of OsARF12 gene may be the target site of miR167d. In order to prove this, semiquantitative RT-PCR (sqRT-PCR) and quantitative RT-PCR (qRT-PCR) techniques were used to analyze the expression of OSARF12 in tobacco and rice callus, and it was found that Osa-miRNA167d inhibited OsARF12 [47]. It shows that OsARF12 is regulated by miR167d and is a post-transcriptional event. Researchers constructed the target mimetic expression of Osa-miR167d (MIM167d) and established a reporting system based on yellow fluorescent protein (YFP), further indicating that OsARF12 is the target site of Osa-miR167d [20].

IAR3 is the target gene of miR167 [48], IAR3 is a member of the amide hydrolase family, and the IAA amide hydrolase family of Arabidopsis thaliana contains seven genes, including IAR3, ILL1, ILL2, ILL3, ILL5, ILL6 and ILR1 [49]. IAR3, a hydrolase encoding IAA-Ala, can release a biologically active auxin (IAA) from inactive IAA-Ala, regulate auxin balance in plants, and is induced by jasmonic acid (JA) [50]. It is most strongly expressed in roots, stems and flowers. IAR3 is a regulator of root structure under osmotic stress and drought stress. miR167 targets IAR3 on root development and stress defense response. In addition, AIRP2 may be the target gene of miR167 [26]. AIRP2 is a circular E3 ubiquitin ligase [51]. In the early stage of somatic embryogenesis in longan, miR167 may regulate the morphology of early somatic embryogenesis by regulating AIRP2. Brassica napus miR167 cleaves BnNRAMP1b transcripts [25]. NRAMPs are membrane transporters responsible for the distribution of metals in plants [52, 53]. Cadmium stress promotes the effects of BnNRAMP1b and miR167. The differential expression pattern verifies that BnNRAMP1b is the target gene of miR167.

4. Biological functions of miR167 family

4.1 miR167 regulates the development of roots, stems and leaves

In the process of plant growth and development, lateral roots are crucial for plants to absorb water and mineral elements, and the development of lateral roots is affected by many factors, auxin can integrate intrinsic and extrinsic environmental signals to regulate lateral root development [54]. miR167 is involved in auxin signaling. GH3 is a member of the auxin responsive gene family, and GH3 protein has the adenylation function of IAA, salicylic acid or jasmonic acid (JA), regulation of cell free IAA by binding with IAA [55]. miR167 participates in the miR167-ARF8-OsGH3-2 signaling pathway, and regulates GH3 family members in the downstream by targeting ARF8 [46, 56]. miR167-ARF8 circuit mediates plant lateral root initiation and morphogenesis, regulates plant response to nitrogen [6]. High nitrogen treatment before Arabidopsis thaliana lateral root germination inhibited the expression of miR167a, and promotes ARF8 transcription accumulation after nitrogen treatment. In addition, miR167 interacts with other miRNAs, helping to fine tune the number of adventitious roots in plants. ARF6 and ARF8 interacted with ARF17 as positive and negative regulators of adventitious root initiation, and regulated each other’s expression at transcriptional and posttranscriptional levels by regulating miR160 and miR167 [7]. At the same time, based on the cucumber mosaic virus strain ZMBJ (ZMBJ-CMV), the ZMBJ-CMV-2bN81-STTM vector was newly developed to express a short tandem target mimic (STTM). Researchers used ZMBJ-CMV-STTM167 to down-regulate Zma-miR167 in corn, resulting in a significant reduction in the number and length of lateral roots [57].

The root development of leguminous plants has special function, because of the invasion and specialization of rhizobia, the lateral root nodules are produced, and the symbiotic nitrogen fixation is used to obtain the nitrogen nutrient elements needed for the growth and development of plants [58], increasing the growth of lateral roots and the number of nodules by molecular techniques can affect the nitrogen fixation ability of legumes. Rhizobium induces the expression of miR167c in the endothelial cells of soybean nodules, and can control multiple nodulation genes (ENOD40, NIN, NSP1, HAP2-1, HAP2-2) to actively regulate nodules. Overexpression of miR167c inhibits the activity of GmARF8, weakens the auxin sensitivity of root cortex cells, and promotes the development of root nodules through downstream signals of NF signaling pathway [8]. miR167 may control nodule formation and root morphological structure by inhibiting auxin signal, the nodulation efficiency under low rhizobia has not been verified. It is suggested that miR167 mainly regulates root development through auxin transduction pathway, and miR167-ARF6/8 circuit may be a highly conservative regulatory mechanism in auxin-mediated biological processes during plant root development.

In addition, miR167 is involved in regulating the development of other vegetative organs in plants, such as the overexpression of miR167 in transgenic rice, the transcriptional levels of OsARF6, OsARF12, OsARF17 and OsARF25 will be significantly reduced, resulting in dwarfing of transgenic rice plants and a significant reduction in tiller number [9]. Overexpression of miR167a reduced the length of cells, but the number of cells increased, but the final internodes and leaves shrank [10]. The reduction of miR167 expression had little effect on the number of cells and the size of leaves, but resulted in leaf curling and wrinkling [11]. Studies of miR167’s involvement in plant stems and leaves have been few and far between. miR167 still has many unknown functions to discover.

4.2 miR167 regulates flower development

4.2.1 miR167 regulates plant flowering time

Flowering is the transition from infancy to adulthood of vascular plant, and is the key to plant growth and development and the sustainable development of future generations, which are affected by plant growth and environmental conditions [59, 60]. miR167 (MIM167) target mimic was first obtained from Arabidopsis thaliana by artificial miRNA target mimic technology, which led to ARF gene expression disorder and late flowering phenotype [61]. It was confirmed that miR167 can regulate flowering time of plants. To test this idea, researchers obtained Arabidopsis thaliana miR16a deletion mutant, which also showed late flowering [15]. The expression of miRNA related to flowering and its target genes in 35S-MIM167 tobacco lines with different miR167 expression levels was proportional to the reduction of miR167 [11]. The low level expression of miR167 increased the expression of GA transcription factor MYB, when the expression of MYB was higher than that of AP2, the expression of LFY increased and the expression of AP2 decreased significantly. In the contrary, the high expression of AP2 inhibited the expression of LFY, which led to late flowering [11]. miR319 targets TCP transcription factors involved in plant biological process [62], MYB and TCP regulate miR167 to form miR159-miR167-miR319 network pattern to regulate ARF gene activity, and then play a role in sepals, petals and anthers [63]. Therefore, miR167 directly or with plant flowering time related miRNA co-regulate flowering gene transcription to regulate plant flowering time.

4.2.2 miR167 regulates floral organ development

The normal development of floral organs is essential to the sexual reproduction of flowering plants. There are 5 types of floral organs: sepals, petals, stamens, gynoecium (carpels) and ovules [64, 65]. The deletion of miR167a mutant leads to ovule arrest and anther do not dehiscence in Arabidopsis thaliana. miR167 mainly regulates ARF genes such as ARF6 and ARF8 involved in the development of female and male floral organs [27].

During flower development, anther dehiscence and pollen release are essential for sexual reproduction in flowering plants. ARF genes are essential for cell elongation and anther dehiscence. Too much or too little ARF gene expression will lead to dehiscence defects and male sterility. miR167 was partially complementary to the c-terminal conserved domain of ARF6 and ARF8, and that ARF gene expression was mainly regulated by cutting, and miR167b overexpression was similar to arf6/arf8 double mutant phenotype, the length of filaments became shorter, the anther did not dehisce and the germination rate of pollen decreased [13]. miR167 in terms of anther dehiscence, the miR167a mutant allows ARF6 and ARF8 to promote excessive cell elongation through the auxin signal transduction pathway. Eventually, the overgrowth of anthers affects the drying time of the anthers and causes them to fail to crack [14]. In addition, obtained by gene editing technology to obtain miR167a mutant, further confirming that the anthers become larger and cannot crack, but they produced normal pollen [15].

In addition to Arabidopsis thaliana, the role of miR167 in regulating floral organ development has also been demonstrated in other plants. miR167 targets InARF8 to regulate the pistil development of morning glory (Ipomoea nil) [17]. InARF8 gene has the strongest signal in the vascular bundle region of the cotyledons, further suggesting that ARF gene may be involved in flower organ development by controlling cell elongation. By in situ hybridization of tomato flower buds with SpARF6A and SpARF8B probes, it was found that the ARF gene was strongly expressed in pistil. Overexpression of miR167a resulted in the decrease of SpARF6 and SpARF8 transcripts, possibly down-regulating the termination of Style2.1 delayed inflorescence meristems [10]. In the end, the anthers produce viable pollen, but the stamens and styles of plants are shortened, the pollen can not germinate on the surface of stigma or grow through the style, resulting in female sterility. This is different from the female sterility of Arabidopsis thaliana miR167a mutant and mARF6, which results from the ovule tegument defect and affects the pollen tube to guide the ovule and embryo development [15, 27]. The function of miR167 in floral organ morphogenesis needs further study (Fig. 1).

Figure 1: miR167 regulates pistil development.

4.3 miR167 regulates plant embryo and seed development

Seeds are the descendants of seed plants. High quality seeds promote good economic returns for Cash crop, while seed size is determined by the interaction of the seed coat, embryo, and endosperm [66, 67, 68]. It has been reported that auxin biosynthesis increases in the seed coat early in embryogenesis, and that auxin produced by the mother is essential for embryonic development, and miR167a and miR167b have also been detected in globular embryos[69]. Serendipitously, researchers found that the Arabidopsis thaliana mir167a (♀) with Wild Arabidopsis thaliana (♂) to produce seed coat and endosperm defects, which further proved that miR167a played a role in regulating embryo development [15]. In order to further verify whether the developmental defects of mir167a mutant were caused by overexpression of ARF6 and ARF8. Researchers hybridized the mir167a mutant with arf6 and arf8 double mutant can improve pollen viability and the anther dehiscence defects of mir167a plants were largely rescued. Furthermore, miR167a overexpression suppresses the expression of CsF8 gene in camelina (Camelina sativa) plants, thereby inhibiting CsFAD3 expression and ultimately slightly delaying seed maturation, but increasing seed size [18]. miR167 is highly expressed during seed development in maize and barley (Hordeum vulgare) and may be involved in the metabolic regulation of seed maturation [70, 71]. In addition, the researchers identified a candidate gene, OsAUX3, which controls grain length and grain weight, and identified OsARF6 as an upstream transcription factor for OsAUX3. OsAF6 can directly bind to the auxin response element on the promoter of OsAUX3 to control grain length by changing the longitudinal expansion of grain cells and the distribution and content of auxin [72]. The revealed miR167a-OsARF6-OsAUX3 module plays a key role in regulating rice grain length and grain weight traits.

Somatic embryogenesis (SEG) is regulated by miRNA via plant hormone signaling pathway [73]. At the early stage of somatic embryogenesis, the expression of miR167 decreased significantly at the initial dedifferentiation stage and increased at the late dedifferentiation stage, and was significantly higher in non-embryonic callus than in embryonic callus [74, 75]. miR167 was highly expressed in the late stage of SEG of larch (Larix leptolepis) and longan [76, 77]. miR167 reached the highest level in Citrus reticulata Blanco cotyledonary embryogenesis [78]. The reduction of miR167 activity promoted the formation of corpus callosum and somatic embryogenesis [79]. Auxin is essential for somatic embryogenesis, ARF6 and ARF8 are necessary for auxin gradient reaction, and auxin gradient related expression is activated by selenium [80]. LEC2 is a positive regulator of selenium-induced YUC-mediated auxin biosynthesis in Arabidopsis thaliana somatic embryogenesis [81, 82]. The overexpression of miR167c inhibited the formation of selenium and increases the expression of LEC2 [12], and at the same time interfered with PIN-FORMED1 (PIN1) in cell membrane of embryogenic callus affected auxin transport [83, 84, 85]. miR167 targeted ARF6 and ARF8, effects on auxin synthesis and local auxin transport in embryogenic callus, thus regulating Arabidopsis thaliana somatic embryogenesis.

4.4 miR167 is involved in the regulation of plant stress response

Environmental factors can affect the growth and development of plants. When plants are stimulated by adversity, growth and development are inhibited. Plants coordinate their growth and development to cope with stress through external morphological changes or internal physiological responses. The stress responses of plants mainly include biotic stress such as virus, pathogen, pest, and abiotic stress such as high salt, drought and low temperature. miR167 plays an active role in plant stress response.

4.4.1 miR167 Regulates Plant Biotic Stress

miR167 was differentially expressed in response to biotic stresses, plants may respond to various stresses by regulating miR167. Hibiscus chlorosis ringspot virus [86], cucumber mosaic virus (CMV) and tomato aspergillosis virus (TAV) [87] can all increase the expression of miR167. Cyst nematodes [88] and root knot nematodes (RKN) [89] induced significant down-regulation of miR167. The same stress had different effects on the expression of miR167 at different growth stages, and the expression of miR167 increased firstly and then decreased under the stress of wheat rust [90]. miR167 targets ARF to reduce the influence of soybean mosaic virus (SMV) infection on the growth of soybean [91]. Arabidopsis thaliana miR167a targets ARF6/ARF8, which results in relatively closed leaf stomata to prevent the entry of Pseudomonas syringae [16]. Osa-miR167d deletion mutant promotes the expression of defense and cell death related genes (KS4, PAL, NAC4, PR1a, PBZ1 and PR10b) and increased JA content [92, 93], thereby enhancing the immunity of rice to Magnaporthe oryzae [20]. Solanaceae plant miR167 promotes changes in the expression of IAR3 leading to changes in auxin homeostasis and enhances the defense of plants against pathogens [21]. Fungal or viral infections increase the expression of tomato miR167a and activate the miR167a regulatory mechanism in response to stress [94]. miR167 is differentially expressed under different stress conditions and can respond to biological stress by regulating stoma opening or inducing the expression of downstream defense genes and auxin homeostasis.

4.4.2 miR167 regulates abiotic stresses in plants

miR167 plays a role in abiotic stress and is induced under high salinity and drought stress [95]. UV-B radiation caused an up-regulation of miR167 expression in Populus tremula [96], and miR167 targeted TcARF6 in Tamarix chinensis under salt stress [19]. The expression of miR167 under salt stress was analyzed by microarray hybridization, which was caused by different salt sensitivity of different species, it was found that the expression of miR167 in salt-tolerant cotton was up-regulated compared with that in salt-sensitive cotton [97]. Seven members of the Osa-miR167 gene family were identified to be inhibited by salt stress, which upregulates the expression of OsARF6, promotes lateral root elongation and accumulates more energy to enhance plant stress resistance [98]. Researchers also confirmed this view in salt-tolerant maize. At the early stage of salt stress, the down-regulation of miR167 in salt-tolerant maize resulted in ARF transcription accumulation and regulated the root and stem development to accumulate more biomass to offset the damage caused by salt stress [99]. In addition, under salt stress, miR393, miR167 and ARF formed a network mechanism in response to stress, which stimulated the up-regulation of miR393 and inhibited the release of AUX/IAA, and the up-regulation of miR167 expression induced the decrease of ARF expression, thus, the development of the plant is weakened and the stress tolerance is enhanced [100, 101]. In addition, the expression of miR167 was down-regulated by drought and high temperature, and the expression of miR167 was up-regulated by cold stress [102]. In wheat (Triticum aestivum), the decrease of miR167 induced stomatal closure and increased leaf water content in response to water stress [22]. High osmotic stress stimulated the down-regulation of miR167, and the expression of IAR3 increased. miR167 targets ARF to promote the production of jasmonic acid [92], which is a strong inducer of IAR3. IAR3 regulates the expression of ARF by feedback of IAA content and promotes the interaction between miR167-IAR3 moudle and miR167-ARF6/8 circuit, to enhance the tolerance of plants to osmotic stress [44, 47].

miR167 is expressed differently in different species and under stress stimulation. Plant response to abiotic stress is mainly regulated by auxin signaling pathway. Plants can reduce miR167 expression and increase their energy accumulation to resist adversity, or increasing the expression of miR167 could weaken the development of plants and enhance the tolerance to stress.

5. Application prospect of miR167 in agricultural production

miR167 also has a broad application prospect in agricultural production. It regulates the development of plant reproductive organs, flowering time, seed and fruit development, and stress tolerance, all of which are beneficial to crop production. miR167 is highly expressed in elongation and maturation stage, and may play a role in cell elongation and differentiation [103]. miR167 was abundant in meiotic cells of Arabidopsis thaliana, soybean and cucumber (Cucumis sativus) [104]. miR167-ARF regulates the seed development of Arabidopsis thaliana, camellia, maize, barley [15, 18, 70, 71]. It also regulates the number of tillers in rice and determines the grain yield by auxin pathway or by regulating grain filling [9, 105]. And the miR167a-OsARF6-OsAUX3 module plays a key role in regulating rice grain length and grain weight traits and improving rice yield [72]. miR167 plays an important role in the fruit development of peach (Prunus persica) and the pod development of peanut [106, 107]. The reproductive organ development and flowering time of crops are important for production and breeding. miR167 is involved in regulating flower organ development and flowering time, helping plants transition from vegetative growth stage to reproductive development stage [11, 15].

6. Conclusions and outlook

In recent years, miR167 has been widely studied for its role in regulating plant growth and development and biotic stress. miR167 directly or together with other miRNAs regulates plant growth and development in Arabidopsis thaliana, tobacco, rice, soybean, corn, camellia, longan, wheat. miR167 has been found to regulate many plant development processes, including lateral root, leaf, flowering, reproductive organs, embryo and seed development and response to stress. Therefore, according to the function summary of miR167 in Arabidopsis thaliana and rice, it is helpful to explore the function of miR167 in other crops. However, due to the diversity of plant species, miR167 has not been fully studied in different species. The potential function of miR167 remains to be explored.

6.1 miR167 increases crop yields

Auxin affects all aspects of plant growth and development. The miR167-ARF model is involved in regulating crop seed and fruit development and plant morphology through auxin pathway.

However, miR167 has not been studied in depth in soybean. Whether miR167 regulates peanut pod development can regulate soybean pod is worth studying. Soybeans convert atmospheric nitrogen to ammonia by forming nodules with nitrogen-fixing rhizobia [108]. Nitrogen is an important factor affecting seed yield. Applying nitrogen fertilizer after flowering can promote plant growth and increase nitrogen content and size of single seed significantly [109]. Studies have shown that when Rhizobium does not exist, miR167 members remain at a low level, while rhizobium induces a strong expression of miR167 [8, 110]. miR167c-GmARF8 may be an effective method to improve the nodulation efficiency of soybean in the absence of rhizobia. Inoculating rhizobia to increase the number of soybean nodules and thus improve soybean yield has become a conventional way of soybean cultivation [111, 112, 113]. Editing miR167 by molecular techniques to increase the number of lateral roots and nodules of soybean plants, to promote plant growth and yield through symbiotic nitrogen fixation. It is beneficial to reduce the use of nitrogen fertilizer to protect the environment has good economic benefits. Could this method also be applied to other legumes to increase crop yields? Therefore, in-depth study of the regulation mechanism between miR167 and crop yield, and breeding of fine varieties through biological breeding will help to play an active role in agricultural production of miR167.

6.2 miR167 and its prospect in disease resistance research

In agricultural production, the impact of pests and diseases on crops is huge, and the main way to resist crop pests and diseases is through spraying pesticides. However, now people are increasingly pursuing organic green products, it has become the trend of the times to strengthen the defense ability of plants against diseases and insect pests by biotechnology. miR167-ARF pattern is known to enhance the immunity of soybean, wheat, rice and other important crops against diseases and pests, or miR167-IAR3 can enhance the defense ability of solanaceous plants against pathogens and pests. Whether miR167 can be applied to other important crops, such as peanuts and corn, to enhance the defense against pests and diseases and obtain economic benefits. It is still needs further exploration and research.

6.3 Future application of miR167 in plant stress resistance

The expression of miR167 was increased or decreased under different adversity conditions. ARF or IAR3 could accumulate energy by auxin pathway or weaken the development of plants to enhance the tolerance to stress. miR167 is responsive to high salinity, drought and low temperature stress, and these environmental factors are the main environmental factors that limit crop yield and affect food security. For saline-alkali land, planting halophytes can improve different types of saline soil [114]. Therefore, it is significant to obtain stress-resistant crops. It has been reported that miR167 targets ARF in response to salt stress in Tamarix ramosissima and salt-tolerant maize, which means that the miR167-ARF model can be established to enhance the salt tolerance of plants. It is possible to obtain more salt-tolerant crops, such as rice and soybeans, to expand the planting area of cash crops, and to effectively use saline land.

6.4 Effects of plant hormones on miR167

Plant hormones are a group of small molecules with various structures, including jasmonates, salicylates, abscisates, auxin, gibberellins, and cytokinin, in which auxin is involved in many processes of plant growth. ARF interacts with AUX/IAA gene in signal transduction pathway and participates in plant hormone signaling pathway [115, 116]. miR167-targeted ARFs participates in the miR167-ARF8-OSGH3-2 signaling pathway, which affects the level of IAA and responds to the presence of exogenous auxin. Exogenous auxin rapidly promotes the expression of miR167, thereby affects the expression of downstream genes. However, it seems that other plant hormones, such as Cytokinin, abscisic acid and gibberellin, have no obvious effect on miR167. Whether auxin’s effect on miR167 expression is direct still needs further investigation.

6.5 Study on miR167 target gene mechanism model by gene editing technique

Genome editing technology is a powerful tool for studying gene function and crop improvement. Among them, CRISPR/Cas9 and base editing (BE) are widely used in functional genomics and precise molecular breeding of crops. CRISPR/Cas9 is a genome-directed editing technique mediated by guide RNA [117, 118, 119]. The technique has been widely used in biology and crop genetics and breeding, and the CRISPR/Cas9 technique has unique advantages. It has simple operation and high editing efficiency and has become the main gene editing technique at present. The improved base-editing technology of CRISPR-Cas9 system can achieve high-precision target gene editing without double-stranded DNA cleavage. The conversion of pyrimidine-pyrimidine (CBE), purine-purine (ABE), pyrimidine-purine (CGBE1 or miniCGBE1) can be realized by base editing tools [120, 121, 122]. Considering that with the development of CRISPR/Cas9 and base editing technology, miR167 and downstream target genes are edited to explore and improve the understanding of interaction mechanism between miR167 and target genes, thereby obtain high quality or high resistance germplasm resources. This will be a big step forward in agricultural production.

7. Author contributions

XL wrote this manuscript; SH participated in the writing and modification of this manuscript; HTX conceptualized the idea. All authors have read and agreed to the published version of the manuscript.

8. Ethics approval and consent to participate

Not applicable.

9. Acknowledgment

Not applicable.

10. Funding

This research received no external funding.

11. Conflict of interest

The authors declare no conflict of interest, and the Bellagen Biotechnology Co., Ltd has no conflict of interest with this paper.

References
  • [1] Song X, Li Y, Cao X, Qi Y. MicroRNAs and their Regulatory Roles in Plant–Environment Interactions. Annual Review of Plant Biology. 2019; 70: 489–525.
  • [2] Liu SR, Zhou JJ, Hu CG, Wei CL, Zhang JZ. MicroRNA-Mediated Gene Silencing in Plant Defense and Viral Counter-Defense. Frontiers in Microbiology. 2017; 8: 1801.
  • [3] Sun X, Lin L, Sui N. Regulation mechanism of microRNA in plant response to abiotic stress and breeding. Molecular Biology Reports. 2019; 46: 1447–1457.
  • [4] Stepien A, Knop K, Dolata J, Taube M, Bajczyk M, Barciszewska-Pacak M, et al. Posttranscriptional coordination of splicing and miRNA biogenesis in plants. Wiley Interdisciplinary Reviews RNA. 2017; 8: e1403.
  • [5] Pu M, Chen J, Tao Z, Miao L, Qi X, Wang Y, et al. Regulatory network of miRNA on its target: coordination between transcriptional and post-transcriptional regulation of gene expression. Cellular and Molecular Life Sciences. 2019; 76: 441–451.
  • [6] Gifford ML, Dean A, Gutierrez RA, Coruzzi GM, Birnbaum KD. Cell-specific nitrogen responses mediate developmental plasticity. Proceedings of the National Academy of Sciences of the United States of America. 2008; 105: 803–808.
  • [7] Gutierrez L, Bussell JD, Păcurar DI, Schwambach J, Păcurar M, Bellini C. Phenotypic Plasticity of Adventitious Rooting in Arabidopsis is Controlled by Complex Regulation of AUXIN RESPONSE FACTOR Transcripts and MicroRNA Abundance. Plant Cell. 2009; 21: 3119–3132.
  • [8] Wang Y, Li K, Chen L, Zou Y, Liu H, Tian Y, et al. MicroRNA167-Directed Regulation of the Auxin Response Factors GmARF8a and GmARF8b is Required for Soybean Nodulation and Lateral Root Development. Plant Physiology. 2015; 168: 984–999.
  • [9] Liu H, Jia S, Shen D, Liu J, Li J, Zhao H, et al. Four AUXIN RESPONSE FACTOR genes downregulated by microRNA167 are associated with growth and development in Oryza sativa. Functional Plant Biology. 2012; 39: 736.
  • [10] Liu N, Wu S, Van Houten J, Wang Y, Ding B, Fei Z, et al. Down-regulation of AUXIN RESPONSE FACTORS 6 and 8 by microRNA 167 leads to floral development defects and female sterility in tomato. Journal of Experimental Botany. 2014; 65: 2507–2520.
  • [11] Arora S, Pandey DK, Chaudhary B. Target-mimicry based diminution of miRNA167 reinforced flowering-time phenotypes in tobacco via spatial-transcriptional biases of flowering-associated miRNAs. Gene. 2019; 682: 67–80.
  • [12] Su YH, Liu YB, Zhou C, Li XM, Zhang XS. The microRNA167 controls somatic embryogenesis in Arabidopsis through regulating its target genes ARF6 and ARF8. Plant Cell, Tissue and Organ Culture. 2015; 124: 405–417.
  • [13] Ru P, Xu L, Ma H, Huang H. Plant fertility defects induced by the enhanced expression of microRNA167. Cell Research. 2006; 16: 457–465.
  • [14] Zheng L, Nagpal P, Villarino G, Trinidad B, Bird L, Huang Y, et al. miR167 limits anther growth to potentiate anther dehiscence. Development. 2019; 146: dev174375.
  • [15] Yao X, Chen J, Zhou J, Yu H, Ge C, Zhang M, et al. An Essential Role for miRNA167 in Maternal Control of Embryonic and Seed Development. Plant Physiology. 2019; 180: 453–464.
  • [16] Caruana JC, Dhar N, Raina R. Overexpression of Arabidopsis microRNA167 induces salicylic acid-dependent defense against Pseudomonas syringae through the regulation of its targets ARF6 and ARF8. Plant Direct. 2020; 4: e00270.
  • [17] Glazińska P, Wojciechowski W, Wilmowicz E, Zienkiewicz A, Frankowski K, Kopcewicz J. The involvement of InMIR167 in the regulation of expression of its target gene InARF8, and their participation in the vegetative and generative development of Ipomoea nil plants. Journal of Plant Physiology. 2014; 171: 225–234.
  • [18] Na G, Mu X, Grabowski P, Schmutz J, Lu C. Enhancing microRNA167A expression in seed decreases the alpha-linolenic acid content and increases seed size in Camelina sativa. Plant Journal. 2019; 98: 346–358.
  • [19] Ye Y, Wang J, Wang W, Xu LA. ARF family identification in Tamarix chinensis reveals the salt responsive expression of TcARF6 targeted by miR167. PeerJ. 2020; 8: e8829.
  • [20] Zhao ZX, Feng Q, Cao XL, Zhu Y, Wang H, Chandran V, et al. Osa-miR167d facilitates infection of Magnaporthe oryzae in rice. Journal of Integrative Plant Biology. 2020; 62: 702–715.
  • [21] D’Ippolito S, Vankova R, Joosten MHAJ, Casalongué CA, Fiol DF. Knocking down expression of the auxin-amidohydrolase IAR3 alters defense responses in Solanaceae family plants. Plant Science. 2016; 253: 31–39.
  • [22] Fileccia V, Ingraffia R, Amato G, Giambalvo D, Martinelli F. Identification of microRNAS differentially regulated by water deficit in relation to mycorrhizal treatment in wheat. Molecular Biology Reports. 2019; 46: 5163–5174.
  • [23] Barik S, Kumar A, Sarkar Das S, Yadav S, Gautam V, Singh A, et al. Coevolution Pattern and Functional Conservation or Divergence of miR167s and their targets across Diverse Plant Species. Scientific Reports. 2015; 5: 14611.
  • [24] Kozomara A, Griffiths-Jones S. MiRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Research. 2011; 39: D152–D157.
  • [25] Meng JG, Zhang XD, Tan SK, Zhao KX, Yang ZM. Genome-wide identification of Cd-responsive NRAMP transporter genes and analyzing expression of NRAMP 1 mediated by miR167 in Brassica napus. Biometals. 2017; 30: 917–931.
  • [26] Wang JY, Shen X, Chen XH, Xu X, Zhang S, Su L, et al. Molecular characteristics of longan miR167 family and expression patterns of potential targets in early somatic embryogenesis. Chinese Journal of Applied and Environmental Biology. 2021; 27: 146–157. (In Chinese)
  • [27] Wu M, Tian Q, Reed JW. Arabidopsis microRNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction. Development. 2006; 133: 4211–4218.
  • [28] Hagen G. Auxin signal transduction. Essays in Biochemistry. 2015; 58: 1–12.
  • [29] Li YL, Gao ZH, Song J, et al. Auxin Response Factor ARF and Growth and Development. Acta Plant Physiology. 2017; 053: 1842–1858.
  • [30] Chandler JW. Auxin response factors. Plant, Cell & Environment. 2016; 39: 1014–1028.
  • [31] Roosjen M, Paque S, Weijers D. Auxin Response Factors: output control in auxin biology. Journal of Experimental Botany. 2018; 69: 179–188.
  • [32] Luo J, Zhou J, Zhang J. Aux/IAA Gene Family in Plants: Molecular Structure, Regulation, and Function. International Journal of Molecular Sciences. 2018; 19: 259.
  • [33] Guilfoyle TJ, Hagen G. Auxin response factors. Current Opinion in Plant Biology. 2007; 10: 453–460.
  • [34] Okushima Y, Overvoorde PJ, Arima K, Alonso JM, Chan A, Chang C, et al. Functional genomic analysis of the AUXIN RESPONSE FACTOR gene family members in Arabidopsis thaliana: unique and overlapping functions of ARF7 and ARF19. Plant Cell. 2005; 17: 444–463.
  • [35] Wang D, Pei K, Fu Y, Sun Z, Li S, Liu H, et al. Genome-wide analysis of the auxin response factors (ARF) gene family in rice (Oryza sativa). Gene. 2007; 394: 13–24.
  • [36] Wu J, Wang F, Cheng L, Kong F, Peng Z, Liu S, et al. Identification, isolation and expression analysis of auxin response factor (ARF) genes in Solanum lycopersicum. Plant Cell Reports. 2011; 30: 2059–2073.
  • [37] Xing H, Pudake RN, Guo G, Xing G, Hu Z, Zhang Y, et al. Genome-wide identification and expression profiling of auxin response factor (ARF) gene family in maize. BMC Genomics. 2011; 12: 178.
  • [38] Mun J, Yu H, Shin JY, Oh M, Hwang H, Chung H. Auxin response factor gene family in Brassica rapa: genomic organization, divergence, expression, and evolution. Molecular Genetics and Genomics. 2012; 287: 765–784.
  • [39] Ha CV, Le DT, Nishiyama R, Watanabe Y, Sulieman S, Tran UT, et al. The auxin response factor transcription factor family in soybean: genome-wide identification and expression analyses during development and water stress. DNA Research. 2013; 20: 511–524.
  • [40] Finet C, Berne-Dedieu A, Scutt CP, Marlétaz F. Evolution of the ARF gene family in land plants: old domains, new tricks. Molecular Biology and Evolution. 2013; 30: 45–56.
  • [41] Sun Z, Huang K, Han Z, Wang P, Fang Y, Genome-wide identification of Arabidopsis long noncoding RNAs in response to the blue light. Scientific Reports. 2020; 10: 6229.
  • [42] Weijers D, Nemhauser J, Yang Z. Auxin: small molecule, big impact. Journal of Experimental Botany. 2018; 69: 133–136.
  • [43] Yang J, Tian L, Sun M, Huang X, Zhu J, Guan Y, et al. AUXIN RESPONSE FACTOR17 is essential for pollen wall pattern formation in Arabidopsis. Plant Physiology. 2014; 162: 720–731.
  • [44] Nagpal P, Ellis CM, Weber H, Ploense SE, Barkawi LS, Guilfoyle TJ, et al. Auxin response factors ARF6 and ARF8 promote jasmonic acid production and flower maturation. Development. 2005; 132: 4107–4118.
  • [45] Mao Z, He S, Xu F, Wei X, Jiang L, Liu Y, et al. Photoexcited CRY1 and phyB interact directly with ARF6 and ARF8 to regulate their DNA-binding activity and auxin-induced hypocotyl elongation in Arabidopsis. New Phytologist. 2020; 225: 848–865.
  • [46] Tian C, Muto H, Higuchi K, Matamura T, Tatematsu K, Koshiba T, et al. Disruption and overexpression of auxin response factor 8 gene of Arabidopsis affect hypocotyl elongation and root growth habit, indicating its possible involvement in auxin homeostasis in light condition. Plant Journal. 2004; 40: 333–343.
  • [47] Qi Y, Wang S, Shen C, Zhang S, Chen Y, Xu Y, et al. OsARF12, a transcription activator on auxin response gene, regulates root elongation and affects iron accumulation in rice (Oryza sativa). New Phytologist. 2012; 193: 109–120.
  • [48] Kinoshita N, Wang H, Kasahara H, Liu J, Macpherson C, Machida Y, et al. IAA-Ala Resistant3, an evolutionarily conserved target of miR167, mediates Arabidopsis root architecture changes during high osmotic stress. Plant Cell. 2012; 24: 3590–3602.
  • [49] Widemann E, Miesch L, Lugan R, Holder E, Heinrich C, Aubert Y, et al. The amidohydrolases IAR3 and ILL6 contribute to jasmonoyl-isoleucine hormone turnover and generate 12-hydroxyjasmonic acid upon wounding in Arabidopsis leaves. Journal of Biological Chemistry. 2013; 288: 31701–31714.
  • [50] Davies RT, Goetz DH, Lasswell J, Anderson MN, Bartel B. IAR3 encodes an auxin conjugate hydrolase from Arabidopsis. Plant Cell. 1999; 11: 365–376.
  • [51] Oh TR, Kim JH, Cho SK, Ryu MY, Yang SW, Kim WT. AtAIRP2 E3 Ligase Affects ABA and High-Salinity Responses by Stimulating its ATP1/SDIRIP1 Substrate Turnover. Plant Physiology. 2017; 174: 2515–2531.
  • [52] Thomine S, Wang R, Ward JM, Crawford NM, Schroeder JI. Cadmium and iron transport by members of a plant metal transporter family in Arabidopsis with homology to Nramp genes. Proceedings of the National Academy of Sciences. 2000; 97: 4991–4996.
  • [53] Cailliatte R, Schikora A, Briat J, Mari S, Curie C. High-affinity manganese uptake by the metal transporter NRAMP1 is essential for Arabidopsis growth in low manganese conditions. Plant Cell. 2010; 22: 904–917.
  • [54] Vilches-Barro A, Maizel A. Talking through walls: mechanisms of lateral root emergence in Arabidopsis thaliana. Current Opinion in Plant Biology. 2015; 23: 31–38.
  • [55] Hagen G, Guilfoyle T. Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Molecular Biology. 2002; 49: 373–385.
  • [56] Yang JH, Han SJ, Yoon EK, Lee WS. ‘Evidence of an auxin signal pathway, microRNA167-ARF8-GH3, and its response to exogenous auxin in cultured rice cells’. Nucleic Acids Research. 2006; 34: 1892–1899.
  • [57] Liu X, Liu S, Wang R, Chen X, Fan Z, Wu B, et al. Analyses of MiRNA Functions in Maize Using a Newly Developed ZMBJ-CMV-2bN81-STTM Vector. Frontiers in Plant Science. 2019; 10: 1277.
  • [58] Li KX, Qu DJ, Huang HM, et al. Research progress on molecular mechanisms of miRNA regulation of soybean root nodulation and symbiotic nitrogen fixation. Acta Phytophysiology. 2019; 000: 1587–1594.
  • [59] Bäurle I, Dean C. The Timing of Developmental Transitions in Plants. Cell. 2006; 125: 655–664.
  • [60] Xu M, Hu T, Zhao J, Park M, Earley KW, Wu G, et al. Developmental Functions of miR156-Regulated SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) Genes in Arabidopsis thaliana. PLoS Genetics. 2016; 12: e1006263.
  • [61] Todesco M, Rubio-Somoza I, Paz-Ares J, Weigel D. A collection of target mimics for comprehensive analysis of microRNA function in Arabidopsis thaliana. PLoS Genetics. 2010; 6: e1001031.
  • [62] Ori N, Cohen AR, Etzioni A, Brand A, Yanai O, Shleizer S, et al. Regulation of LANCEOLATE by miR319 is required for compound-leaf development in tomato. Nature Genetics. 2007; 39: 787–791.
  • [63] Rubio-Somoza I, Weigel D. Coordination of flower maturation by a regulatory circuit of three microRNAs. PLoS Genetics. 2013; 9: e1003374.
  • [64] Krizek BA, Fletcher JC. Molecular mechanisms of flower development: an armchair guide. Nature Reviews Genetics. 2005; 6: 688–698.
  • [65] Coen ES, Meyerowitz EM. The war of the whorls: genetic interactions controlling flower development. Nature. 1991; 353: 31–37.
  • [66] Robert HS, Park C, Gutièrrez CL, Wójcikowska B, Pěnčík A, Novák O, et al. Maternal auxin supply contributes to early embryo patterning in Arabidopsis. Nature Plants. 2018; 4: 548–553.
  • [67] Orozco-Arroyo G, Paolo D, Ezquer I, Colombo L. Networks controlling seed size in Arabidopsis. Plant Reproduction. 2015; 28: 17–32.
  • [68] Li N, Xu R, Li Y. Molecular Networks of Seed Size Control in Plants. Annual Review of Plant Biology. 2019; 70: 435–463.
  • [69] Armenta-Medina A, Lepe-Soltero D, Xiang D, Datla R, Abreu-Goodger C, Gillmor CS. Arabidopsis thaliana miRNAs promote embryo pattern formation beginning in the zygote. Developmental Biology. 2017; 431: 145–151.
  • [70] Li D, Liu Z, Gao L, Wang L, Gao M, Jiao Z, et al. Genome-Wide Identification and Characterization of microRNAs in Developing Grains of Zea mays L. PLoS ONE. 2016; 11: e0153168.
  • [71] Bai B, Shi B, Hou N, Cao Y, Meng Y, Bian H, et al. MicroRNAs participate in gene expression regulation and phytohormone cross-talk in barley embryo during seed development and germination. BMC Plant Biology. 2017; 17: 150.
  • [72] Qiao J, Jiang H, Lin Y, Shang L, Wang M, Li D, et al. A Novel miR167a-OsARF6-OsAUX3 Module Regulates Grain Length and Weight in Rice. Molecular Plant. 2021. (in press)
  • [73] Jin L, Yarra R, Zhou L, Zhao Z, Cao H. MiRNAs as key regulators via targeting the phytohormone signaling pathways during somatic embryogenesis of plants. 3 Biotech. 2020; 10: 495.
  • [74] Sabana AA, Rajesh MK, Antony G. Dynamic changes in the expression pattern of miRNAs and associated target genes during coconut somatic embryogenesis. Planta. 2020; 251: 79.
  • [75] Yang X, Wang L, Yuan D, Lindsey K, Zhang X. Small RNA and degradome sequencing reveal complex miRNA regulation during cotton somatic embryogenesis. Journal of Experimental Botany. 2013; 64: 1521–1536.
  • [76] Zhang J, Zhang S, Han S, Wu T, Li X, Li W, et al. Genome-wide identification of microRNAs in larch and stage-specific modulation of 11 conserved microRNAs and their targets during somatic embryogenesis. Planta. 2012; 236: 647–657.
  • [77] Lin Y, Lai Z. Comparative analysis reveals dynamic changes in miRNAs and their targets and expression during somatic embryogenesis in longan (Dimocarpus longan Lour.). PLoS ONE. 2013; 8: e60337.
  • [78] Wu X, Liu M, Ge X, Xu Q, Guo W. Stage and tissue-specific modulation of ten conserved miRNAs and their targets during somatic embryogenesis of Valencia sweet orange. Planta. 2011; 233: 495–505.
  • [79] Arora S, Singh AK, Chaudhary B. Target-mimicry based miRNA167-diminution ameliorates cotton somatic embryogenesis via transcriptional biases of auxin signaling associated miRNAs and genes. Plant Cell, Tissue and Organ Culture. 2020; 141: 511–531.
  • [80] Su YH, Zhao XY, Liu YB, Zhang CL, O’Neill SD, Zhang XS. Auxin-inducedWUSexpression is essential for embryonic stem cell renewal during somatic embryogenesis in Arabidopsis. Plant Journal. 2009; 59: 448–460.
  • [81] Weijers D, Wagner D. Transcriptional Responses to the Auxin Hormone. Annual Review of Plant Biology. 2016; 67: 539–574.
  • [82] Wójcikowska B, Jaskóła K, Gąsiorek P, Meus M, Nowak K, Gaj MD. LEAFY COTYLEDON2 (LEC2) promotes embryogenic induction in somatic tissues of Arabidopsis, via YUCCA-mediated auxin biosynthesis. Planta. 2013; 238: 425–440.
  • [83] Govindaraju P, Verna C, Zhu T, Scarpella E. Vein patterning by tissue-specific auxin transport. Development. 2020; 147: dev187666.
  • [84] Furutani M, Vernoux T, Traas J, Kato T, Tasaka M, Aida M. PIN-FORMED1 and PINOID regulate boundary formation and cotyledon development in Arabidopsis embryogenesis. Development. 2004; 131: 5021–5030.
  • [85] Yu SX, Zhou LW, Hu LQ, Jiang YT, Zhang YJ, Feng SL, et al. Asynchrony of ovule primordia initiation in Arabidopsis. Development. 2020; 147: dev196618.
  • [86] Gao R, Wan ZY, Wong S. Plant growth retardation and conserved miRNAs are correlated to Hibiscus chlorotic ringspot virus infection. PLoS ONE. 2013; 8: e85476.
  • [87] Feng J, Wang K, Liu X, Chen S, Chen J. The quantification of tomato microRNAs response to viral infection by stem-loop real-time RT-PCR. Gene. 2009; 437: 14–21.
  • [88] Hewezi T, Howe P, Maier TR, Baum TJ. Arabidopsis small RNAs and their targets during cyst nematode parasitism. Molecular Plant-Microbe Interactions. 2008; 21: 1622–1634.
  • [89] Pan X, Nichols RL, Li C, Zhang B. MicroRNA-target gene responses to root knot nematode (Meloidogyne incognita) infection in cotton (Gossypium hirsutum L.). Genomics. 2019; 111: 383–390.
  • [90] Gupta OP, Permar V, Koundal V, Singh UD, Praveen S. MicroRNA regulated defense responses in Triticum aestivum L. during Puccinia graminis f.sp. tritici infection. Molecular Biology Reports. 2012; 39: 817–824.
  • [91] Yin X, Wang J, Cheng H, Wang X, Yu D. Detection and evolutionary analysis of soybean miRNAs responsive to soybean mosaic virus. Planta. 2013; 237: 1213–1225.
  • [92] Ruan J, Zhou Y, Zhou M, Yan J, Khurshid M, Weng W, et al. Jasmonic Acid Signaling Pathway in Plants. International Journal of Molecular Sciences. 2019; 20: 2479.
  • [93] Gupta A, Bhardwaj M, Tran LP. Jasmonic Acid at the Crossroads of Plant Immunity and Pseudomonas syringae Virulence. International Journal of Molecular Sciences. 2020; 21: 7482.
  • [94] Jodder J, Das R, Sarkar D, Bhattacharjee P, Kundu P. Distinct transcriptional and processing regulations control miR167a level in tomato during stress. RNA Biology. 2018; 15: 130–143.
  • [95] Liu HH, Tian X, Li YJ, Wu CA, Zheng CC. Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana. RNA. 2008; 14: 836–843.
  • [96] Jia X, Ren L, Chen Q, Li R, Tang G. UV-B-responsive microRNAs in Populus tremula. Journal of Plant Physiology. 2009; 166: 2046–2057.
  • [97] Li CH, Yin ZJ, Liu YD, et al. Differential expression of miRNA in different salt-tolerant cotton varieties under salt stress. Shandong Agricultural Sciences. 2009 (7):12-17.
  • [98] Meng SJ, Zhang XH, Wang QY, et al. Identification of rice roots in response to salt stress of miRNA and tRF. China Agricultural Sciences. 2020; 053: 669–682.
  • [99] Ding D, Zhang L, Wang H, Liu Z, Zhang Z, Zheng Y. Differential expression of miRNAs in response to salt stress in maize roots. Annals of Botany. 2009; 103: 29–38.
  • [100] Tan X, Calderon-Villalobos LIA, Sharon M, Zheng C, Robinson CV, Estelle M, et al. Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature. 2007; 446: 640–645.
  • [101] Li XY, Cui J, Li JL, et al. Research status of miRNA regulation of plant stress resistance. Jiangsu Agricultural Sciences. 2019; 47: 63–66.
  • [102] Wang LL, Zhao TL, Ge JT, et al. Application prospects of miRNAs in response to plant cold stress in the research of plant cold resistance. Shanghai Journal of Agricultural Sciences. 2017; 33: 129–134.
  • [103] Aydinoglu F, Lucas SJ. Identification and expression profiles of putative leaf growth related microRNAs in maize (Zea mays L.) hybrid ADA313. Gene. 2019; 690: 57–67.
  • [104] Huang J, Wang C, Li X, Fang X, Huang N, Wang Y, et al. Conservation and Divergence in the Meiocyte sRNAomes of Arabidopsis, Soybean, and Cucumber. Plant Physiology. 2020; 182: 301–317.
  • [105] Peng T, Teotia S, Tang G, Zhao Q. MicroRNAs meet with quantitative trait loci: Small powerful players in regulating quantitative yield traits in rice. WIREs RNA. 2019; 10: e1556.
  • [106] Shi M, Hu X, Wei Y, Hou X, Yuan X, Liu J, et al. Genome-Wide Profiling of Small RNAs and Degradome Revealed Conserved Regulations of miRNAs on Auxin-Responsive Genes during Fruit Enlargement in Peaches. International Journal of Molecular Sciences. 2017; 18: 2599.
  • [107] Gao C, Wang P, Zhao S, Zhao C, Xia H, Hou L, et al. Small RNA profiling and degradome analysis reveal regulation of microRNA in peanut embryogenesis and early pod development. BMC Genomics. 2017; 18: 220.
  • [108] Liu A, Ku YS, Contador CA, Lam HM. The Impacts of Domestication and Agricultural Practices on Legume Nutrient Acquisition Through Symbiosis with Rhizobia and Arbuscular Mycorrhizal Fungi. Frontiers in Genetics. 2020; 11: 583954.
  • [109] Kinugasa T, Sato T, Oikawa S, Hirose T. Demand and supply of N in seed production of soybean (Glycine max) at different N fertilization levels after flowering. Journal of Plant Research. 2012; 125: 275–281.
  • [110] Hoang NT, Tóth K, Stacey G. The role of microRNAs in the legume–Rhizobium nitrogen-fixing symbiosis. Journal of Experimental Botany. 2020; 71: 1668–1680.
  • [111] Ulzen J, Abaidoo RC, Mensah NE, Masso C, AbdelGadir AH. Bradyrhizobium Inoculants Enhance Grain Yields of Soybean and Cowpea in Northern Ghana. Frontiers in Plant Science. 2016; 7: 1770.
  • [112] Chibeba AM, Kyei-Boahen S, Guimarães MDF, Nogueira MA, Hungria M. Isolation, characterization and selection of indigenous Bradyrhizobium strains with outstanding symbiotic performance to increase soybean yields in Mozambique. Agriculture, Ecosystems & Environment. 2017; 246: 291–305.
  • [113] Cordeiro CFD, Echer FR. Interactive Effects of Nitrogen-Fixing Bacteria Inoculation and Nitrogen Fertilization on Soybean Yield in Unfavorable Edaphoclimatic Environments. Scientific Reports. 2019; 9: 15606.
  • [114] Ge Y, Luan MJ, Zhang XN, et al., The relationship between the distribution of halophytes and the types of saline-alkali land in China. Journal of Qilu University of Technology. 2021; 35: 14–20.
  • [115] Glauser G, Vallat A, Balmer D. Hormone profiling. Methods in Molecular Biology. 2014; 1062: 597–608.
  • [116] Blázquez MA, Nelson DC, Weijers D. Evolution of Plant Hormone Response Pathways. Annual Review of Plant Biology. 2020; 71: 327–353.
  • [117] Hsu PD, Lander ES, Zhang F. Development and applications of CRISPR-Cas9 for genome engineering. Cell. 2014; 157: 1262–1278.
  • [118] Zhang H, Zhang J, Lang Z, Botella JR, Zhu J. Genome Editing—Principles and Applications for Functional Genomics Research and Crop Improvement. Critical Reviews in Plant Sciences. 2017; 36: 291–309.
  • [119] Chen K, Wang Y, Zhang R, Zhang H, Gao C. CRISPR/Cas Genome Editing and Precision Plant Breeding in Agriculture. Annual Review of Plant Biology. 2019; 70: 667–697.
  • [120] Gaudelli NM, Komor AC, Rees HA, Packer MS, Badran AH, Bryson DI, et al. Programmable base editing of a*T to G*C in genomic DNA without DNA cleavage. Nature. 2017; 551: 464–471.
  • [121] Doudna JA, Charpentier E. Genome editing. the new frontier of genome engineering with CRISPR-Cas9. Science. 2014; 346: 1258096.
  • [122] Komor AC, Kim YB, Packer MS, Zuris JA, Liu DR. Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage. Nature. 2016; 533: 420–424.
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Xia Liu, Sheng Huang, Hongtao Xie. Advances in the regulation of plant development and stress response by miR167. Frontiers in Bioscience-Landmark. 2021. 26(9); 655-665.