23 publications mentioning gma-MIR169p

Open access articles that are associated with the species Glycine max and mention the gene name MIR169p. Click the [+] symbols to view sentences that include the gene name, or the word cloud on the right for a summary.

1

Our results are consistent with the reported upregulation of two NF-YA genes (Glyma02g47380 and Glyma10g10240) [12] that are targeted by miR169 and decreased expression of TEM1 transcription factor [12] that is targeted by miR482.

Our miRNA analysis revealed that the miRNAs targeting above mentioned transcription factors were differentially regulated; miR482 was upregulated while miR169 was downregulated below the stringent threshold level of(log2) fold change (Additional file 2).

Interestingly, miR169 regulation differs between drought tolerant and drought sensitive soybean genotypes; it is downregulated in a tolerant genotype while upregulated in a sensitive genotype [8, 9].

Under Pi deficiency downregulation of miR169 and miR159 whereas upregulation of miR482 and miR397 was reported [32] and similar responses were found during water deficit (Table  2 and Additional file 2).

Magellan in this study, thus the observed miR169 downregulation is consistent (Additional file 2) with the previous reports [9].

Magellan in this study, thus the observed miR169 downregulation (Additional file 2) is consistent with the previous reports [9].

Recently, several studies reported differential expression of miRNAs such as miR164, miR169, miR171, miR396, miR398, miR399, miR408 and miR2118 in drought-stressed plants but their regulation (up or down) differed between different plant species [5].

Among the highly conserved 23 miRNA families [23], two (miR156 and miR166) were classified as high, three (miR168, miR396 and miR172) as moderate and seven (miR169, miR171, miR164, miR390, miR159, miR160 and miR167) as low and two (miR395 and miR399) as extremely low abundantly expressed miRNA families in primary root tips of soybean.

Nineteen miRNA families (miR5767, miR4345, miR169, miR2109, miR482, miR2119, miR2118, miR171, miR164, miR4413, miR390, miR1514, miR159, miR160, miR5781, miR167, miR5373 and miR4409) displayed lower abundances (1000 to 10,000 RPTM) (Additional file 2).

2

Under short-term low N condition, miR160, miR168, miR169, miR319, miR395, and miR399 were up-regulated in roots, while in maize leaves miR172 were up-regulated and miR397, miR398, and miR827 were down-regulated.

Recently, Xu et al. studied detailed response of miRNAs to low N availability in maize shoots and roots at the whole genome level and found that under long-term low N condition, miR167, miR169, miR395, miR399, miR408, and miR528 were down-regulated in maize roots, and in maize leaves miR164, miR172, and miR827 were up-regulated while miR169, miR397, miR398, miR399, miR408, and miR528 were down-regulated.

Interestingly, different species in the miR169 family showed different expression patterns, such as miR169e/f/g/h were down-regulated, while miR169i/j/k/p were up-regulated [30].

Another study indicated that miR156 was up-regulated by low N in Arabidopsis, whereas miR169, miR395 and miR398 were down-regulated [29].

We found that multiple members of the gma-miR169 family were repressed in both roots and shoots of these two soybean varieties under low N stress, and some members of gma-miR398 family were down-regulated only in soybean shoots, while gma-miR395 family were not responsive to low N stress.

Under N limitation, several pri-miR169 species as well as pri-miR398a decreased in Arabidopsis seedlings, whereas several pri-miR156 species and pri-miR447c were found to be induced [29].

Nine miRNA families (miR164, miR169, miR172, miR397, miR398, miR399, miR408, miR528, and miR827) and nine miRNA families (miR160, miR167, miR168, miR169, miR319, miR395, miR399, miR408, and miR528) were identified to respond to low N in maize shoots and roots respectively [30].

3

In Arabidopsis, the expression of miR165/166, miR319c and miR169 is induced by cold stress [8, 9], while in Brachypodium, the expression of both miR172 and miR397 is up-regulated by cold treatment [10].

By contrast, some specific members of the miR169 family are downregulated by cold treatment (e. g., miR169f/j/h/i in Populus and miR169d in Poncirus) [49, 51].

For example, miR169 is upregulated under cold stress in Arabidopsis, Brachypodium and rice [8, 10, 48, 50].

MtHAP2-1, which encodes a transcription factor belonging to the NFY-A family and which is targeted by miR169, has been shown to be required for nodule development [70].

It is likely that HAP2-like genes function as targets of miR169 to regulate cold responses (i. e., nitrogenase activity) in nodules.

Combier J. P. Frugier F. de Billy F. Boualem A. El-Yahyaoui F. Moreau S. Vernie T. Ott T. Gamas P. Crespi M. MtHAP2-1 is a key transcriptional regulator of symbiotic nodule development regulated by microRNA169 in Medicago truncatula Gene.

In many plants, miR169 targets HAP2, which encodes a HAP2 transcription factor subunit and a component of the hetero-trimeric CCAAT-box -binding factor complex (CBF/NF-Y/HAP), which binds the CCAAT motif present in many eukaryotic promoters [69].

However, the targeting of HAP2-like genes by miR169 has not been reported.

Among the eleven cold-responsive miRNAs we identified, four (miR166, miR171, miR2111 and miR169) are highly conserved in higher plants, and these miRNAs have been shown to regulate plant cold responses [8, 10, 11, 48, 49].

Li Y. Fu Y. Ji L. Wu C. Zheng C. Characterization and expression analysis of the Arabidopsis mir169 family Plant Sci.

4

Despite the absence of a meristem in soybean nodules, two targets of miR169, Glyma10g10240 and Glyma17g05920, which encode HAP proteins were highly expressed in the nodules (Figure 5E-F).

miR169 (two different mature forms, 169c and g) was chosen for its previously identified role in nodulation [31]; miR2118/2218 as part of a legume specific family [25]; two new miRNAs identified in this study and four other miRNAs (for which expression data was not available) were randomly selected (see Additional file 2: Figures S4, for dissociation curves and amplification efficiency).

More interestingly, the expression of miR169 genes was very low in nodules.

The organization of MIR169 and MIR169-like genes in these regions (Figure 2) indicates that both regions might have had same number of MIR169-like genes and possible “birth” (e. g. miR169d) and “death” of genes (e. g. MIR169-like genes) occurred more recently, resulting in a diverse set of family members.

We identified four families of miRNAs (miR159, miR169, miR395 and gma-miR-Seq14) that had at least one locus with tandemly duplicated genes.

MIR169 is also organized in cluster in several species including rice [60] and Arabidopsis [61] and its organization highly conserved with G. max[20].

However, unlike MIR169 genes, head to head (MIR159) and tail to tail (MIR395) duplications in addition to tandem duplications were observed in these families (Additional file 2: Figure S2).

A. Illustration showing a portion of soybean chromosome 15 and its paralogous genomic locus on chromosome 9 with tandemly duplicated MIR169 genes (filled arrows), MIR169-like genes (hollow arrows; see text for explanation) and protein-coding genes (grey arrows).

Figure 2 Tandem duplication of MIR169 genes.

However, both regions contain a number of ‘MIR169-like’ genes from which either no mature miRNA has been detected or the ones detected did not fit the criteria established by Meyers et al. [17].

It should be noted that MIR159, MIR169 and MIR395 genes are tandemly duplicated in other plant species as well (e. g. M. truncatula Arabidopsis).

We identified four miRNA families that have tandemly duplicated members: MIR159, MIR169, MIR395, three conserved families, and MIR-Seq14 that is soybean-specific.

C. List of all mature sequences identified for miR169 family (See Table S1 for updated miRbase IDs for miR169 family members).

A number of the paralogous MIR169-like genes had highest similarity to MIR169e, suggesting that they all might have originated form the same precursor.

B. Phylogenetic tree obtained by aligning the precursor sequences of all soybean MIR169 genes.

5

MiR169 was up-regulated in the sensitive cultivar, but down-regulated in the tolerant.

MiR169 targeted nuclear factor Y subunit, which can regulate expression level of some stress-responsive genes [65].

MiR171c and miR319 were highly induced by SCN infection in both cultivars, expression of miR390b was induced in HB specific while miR862, miR5372 and four members of miR169 were SCN-infection induced only in L10.

MtHAP2-1 is essential for nodule meristematic persistence in M. truncatula, and that miR169 confers spatial and temporal accuracy of nodules development [67].

Furthermore, MtHAP2-1, a new transcription factor of the CCAAT -binding family identified in M. truncatula, is regulated by miR169.

Mtr-miR166, Mtr-miR169 of M. truncatula and three soybean miRNAs, Gma-miR482, Gma-miR1511, Gma-miR1512 have been functionally analysed and associated to rhizobial symbiosis [25], [26], [27].

MiR169 guided regulation of these transcription factors appeared to be important in variety of abiotic stress, including drought, cold, salinity, UV-B radiation, and heat stress [61], [62], [63], [65], [66].

6

We also identified down-regulation of miR169 (Figure 5) shown to play a role in nodulation earlier [35].

The target of miR169, a CCAAT -binding transcription factor MtHAP2-1 has been shown to be critical for nodule development in Medicago truncatula [35].

Down-regulation of a set of miRNAs was also observed in response to B. japonicum (e. g. miR160, miR169).

At least two putative miR169 targets predicted in soybean are highly identical (not shown) to the M. truncatula HAP2-1 functionally shown to play a role in nodulation.

UGAAGCUGCCAGCAUGAUCUU 21 H 168 gma-MIR168 UCGCUUGGUGCAGGUCGGGAA 21 H, N (21 nt) 169 gma-MIR169 CAGCCAAGGAUGACUUGCCGG 21 H, P, N (21 nt) gma-MIR169b CAGCCAAGGAUGACUUGCCGA 21 H, P gma-MIR169c AAGCCAAGGAUGACUUGCCGA 21 H, P 171 gma-MIR171a UUGAGCCGUGCCAAUAUCACG 21 H, P gma-MIR171?

7

In general, miRNAs that are conserved across plants, such as miR156, miR164, miR167 and miR169, target transcription factors (TFs), whereas less-conserved miRNAs target fewer TFs (Additional file 8).

It was reported that five conserved miRNAs (miR159, miR162, miR166, miR390, and miR399) presented similar expression levels in root apexes and nodules, but miR169, miR171, miR393, and miR396 enriched in root tips [41].

NF-YAs, the targets of miR169, participate in N and drought stress responses [50].

Soybean 5 NF-YA transcripts are potentially targeted by miR169 members (Additional file 7).

One last set of results in regards to P nutrition shows that miR778, miR398, miR169 and miR408 are also responsive to P limitation [10, 11].

In this study, the abundance of several miR169 family members (miR169c, miR169p, miR169q, and miR169r) was low yet still detectable in soybean leaves (Table 3), which indicates some roles for these miRNAs in leaves, and stands in contrast to the report that gma-miR169 is abundant in soybean shoot apical meristem (SAM) and undetectable in mature soybean leaves [35].

8

The targets were annotated as Nuclear Factor Y (NFY), which were previously shown to be targeted by miR169 in Arabidopsis [26], [27].

Although only a few cleavage targets of the highly accumulated RC-miRNAs were detected, several RC-miRNAs were shown to possess great potential to guide DNA methylation in both Arabidopsis (RC_ath-miR2112, RC_ath-miR391, RC_ath-miR781, RC_ath-miR782, and RC_ath-miR847) and rice (RC_osa-miR156, RC_osa-miR159, RC_osa-miR169, RC_osa-miR1846, RC_osa-miR2118, and RC_osa-miR535) (Figure 4 and Table S6).

For rice, a large portion of the confirmed targets with compelling cleavage signals in the middle of the binding sites were recognized by the mature RC-miRNAs produced from the precursors RC-osa-MIR169p and RC-osa-MIR169q, which share the identical sequences with osa-miR169b/c and osa-miR169h/i/j/k/l/m (Figure 3, Figure S3 and Table S4).

However, it is hard to tell that either RC-osa-miR169 or osa-miR169, or both exert their cleavage -based regulatory roles.

Similar evidences were obtained for RC-osa-miR169p and RC-osa-miR169q (Data S7).

9

Because these homologs are close together argues against their origin from two different miR169 primary transcripts, although evidence for the expression of these two miR169 homologs in one transcript in the form of an EST is lacking.

At least five families (miR319, miR156/157, miR169, miR165/166 and miR394) were found in more than 40 plant species (Table 1).

Although miRNA clusters are not common in plants, a few miRNA families (miR395, miR399, miR169 and miR1219) have been found to exist as clusters [26, 45- 47].

We also found two tandem miR169 homologs in the same orientation and separated by 250 nt in the cotton genomic clone DX401397.

Our analysis indicated that along with the well-documented clustered organization of miR395, miR156 and miR169 also exist as clusters in several plant species.

Interestingly, miR319, miR156/157, miR169, miR165/166 and miR394 homologs were found in 51, 45, 41, 40 and 40 diverse plant species, respectively (Table 1 and see Additional file 1).

Five miRNA families – miR319, miR156/157, miR169, miR165/166 and miR394 – were found in 51, 45, 41, 40 and 40 diverse plant species, respectively.

We also identified two new members belonging to miR319, miR398 and miR403 families and three new members belonging to miR169 (Table 1).

Two miRNAs belonging to the miR169 family in cotton (46) and Brassica napus (49) have been recently reported.

Additionally, miR169 homologs were found in clusters in Lactuca sativa (DY980357), Populus tremula (CK111070) and Euphorbia esula (DV142897) but not in Arabidopsis or rice.

The results suggest that at least four miRNA families (miR156, miR169, miR395 and miR1219) exist as miRNA clusters in plants.

Thus, we show miRNA gene clustering for miR156 and miR169 loci in diverse plant species.

10

For instance, in previous studies, miR167 was up-regulated in response to the chilling stress in soybean nodules and miR169 was down-regulated 24.

The first category included miRNA families (miR156, miR164, miR169, miR4412 and miR5374) targeting SBP, NAC, NFY, GRAS, bHLH transcription factors, respectively, which are involved in the regulation of gene expression and signal transduction.

11

To our knowledge, the first miRNA reported to regulate nodule development (Combier et al., 2006), was miR169, which acts as a negative regulator of HAP2.

MtHAP2-1 is a key transcriptional regulator of symbiotic nodule development regulated by microRNA169 in Medicago truncatula.

The miR169 [*] cleaved MtBCP1 transcripts coding for an arbuscule-specific protein in mycorrhizal roots whereas cleavage products of a GRAS TF predicted as a target of miR5204 [*] were also sequenced in mycorrhizal roots (Devers et al., 2011).

However, functional analyses of miRNAs remained rare and only two miRNAs, miR169, and miR166, were experimentally associated to nodule development before 2009 (Data Sheet 2; Combier et al., 2006; Boualem et al., 2008).

12

Mtr-miR169 was found to regulate nodule development through regulating expression of transcription factor MtHAP2-1 in Medicago truncatula [31].

, found in Bradyrhizobia inoculated soybean roots [32], and gma-miRNAs, such as miR172, miR169, miR1511, miR156, miR4357, miR4416 etc.

13

The differential expression analyses revealed that MIR166a- 5p, MIR166f, MIR169- 3p, MIR397ab and MIR- Seq13 were dow-regulated in the susceptible genotype during pathogen infection, and equally expressed in the resistant plants.

One new gene was detected in MIR169, MIR172, MIR396 and MIR482 with mature sequences originated from both the 3'and 5'arms (Table 4).

14

For example, miR169, which is known to target NF-YA (nuclear factor-Y subunit alpha) in other species, was found to target the genes encoding flavonol synthase and sulfate transporter.

15

These miRNAs including miR156, miR158, miR165, miR167, miR168, miR169, miR171, miR393, miR394 and miR396 were responsive to salt stress and may fine-tune plant stress responses at multiple levels through targeting the genes with different functions including large sets of genes that encode various transcription factors [15, 19, 20].

Further functional analyses of several miRNAs, such as miR169 and miR393, demonstrate that miRNAs indeed play a key role in plant tolerance to salt stress [21, 22].

16

Calvino and Messing [68] established that miR169 family in Sorghum targets the carboxypeptidase mRNAs.

17

A series of targets for known miRNAs, including gma-miR156, gma-miR159, gma-miR160, gma-miR164, gma-miR167, gma-miR169, gma-miR396, gma-miR398 and gma-miR1514, belong to this class (Tables 3, 4).

18

We detected seven NF transcription factor YA subunit mRNAs specifically in seed coats that are targets of miR169 family members that occur in both seed coats and cotyledons ().

19

MtHAP2-1 is a key transcriptional regulator of symbiotic nodule development regulated by microRNA169 in Medicago truncatula.

20

For example, miR156/157, miR159/319, miR166, miR169, and miR394 have been found in 51, 45, 41, 40, and 40 plant species, respectively [34, 38, 41].

In comparison to other plant species, tae-miR169b in wheat and osa-miR169 in rice were the most frequently sequenced miRNAs while miR156 in rice and wheat exhibited low abundance [46].

21

Furthermore, miR169 and miR171, which are involved in powdery mildew infection in wheat [49], were also significantly induced by SCN in both susceptible and resistant cultivars (Additional file 2: Table S2).

22

miR396, miR166, miR172, miR169 and miR395 were also present at multiple loci in date palm, and these miRNAs had the highest average copy number in the other plant species.

23

Seven miRNA families (miR159, miR162, miR164, miR169, miR395, miR396, and miR397) most likely evolved in the common ancestor of spermatophytes, as they were present in both gymnosperm and angiosperm lineages.