Advertisement

Planta

, Volume 248, Issue 3, pp 545–558 | Cite as

Plant small RNAs: advancement in the understanding of biogenesis and role in plant development

  • Archita Singh
  • Vibhav Gautam
  • Sharmila Singh
  • Shabari Sarkar Das
  • Swati Verma
  • Vishnu Mishra
  • Shalini Mukherjee
  • Ananda K. Sarkar
Review

Abstract

Main conclusion

Present review addresses the advances made in the understanding of biogenesis of plant small RNAs and their role in plant development. We discuss the elaborate role of microRNAs (miRNAs) and trans-acting small interfering RNAs (ta-siRNAs) in various aspects of plant growth and development and highlight relevance of small RNA mobility.

Small non-coding RNAs regulate various aspects of plant development. Small RNAs (sRNAs) of 21–24 nucleotide length are derived from double-stranded RNAs through the combined activity of several biogenesis and processing components. These sRNAs function by negatively regulating the expression of target genes. miRNAs and ta-siRNAs constitute two important classes of endogenous small RNAs in plants, which play important roles in plant growth and developmental processes like embryogenesis, organ formation and patterning, shoot and root growth, and reproductive development. Biogenesis of miRNAs is a multistep process which includes transcription, processing and modification, and their loading onto RNA-induced silencing complex (RISC). RISC-loaded miRNAs carry out post-transcriptional silencing of their target(s). Recent studies identified orthologues of different biogenesis components of novel and conserved small RNAs from different model plants. Although many small RNAs have been identified from diverse plant species, only a handful of them have been functionally characterized. In this review, we discuss the advances made in understanding the biogenesis, functional conservation/divergence in miRNA-mediated gene regulation, and the developmental role of small RNAs in different plant species.

Keywords

Small RNA miRNA ta-siRNA Plant development Root development Shoot development 

Introduction

Small RNAs (sRNAs) are non-coding RNA (ncRNA) fragments, which regulate the post-transcriptional silencing of target genes either through transcript cleavage or by translational inhibition (Axtell 2013). Various classes of sRNAs have been reported which differ from each other on the basis of biogenesis pathways (Chen 2009). Based on the precursor sequence, sRNAs can be classified as: miRNAs, ta-siRNAs and heterochromatin-associated (hc-siRNAs) (Axtell 2013). miRNAs and ta-siRNAs are two important classes of plant sRNAs, which control plant growth and development by negatively regulating the expression of their target genes, mostly through transcriptional cleavage (Chen 2012). On the other hand, hc-siRNAs are involved in carrying out the epigenetic modifications of chromatin in the target loci, thus leading to transcriptional gene silencing (Axtell 2013).

miRNAs are well-studied subset of hairpin RNAs defined by the highly precise excision of one or more functional products, which are called as mature miRNAs. miRNAs were first discovered as regulators of developmental timing in Caenorhabditis elegans (Lim et al. 2003). miRNAs are conserved over long evolutionary distances suggesting the role of an evolutionarily conserved mechanism of miRNA-mediated gene regulation (Molnar et al. 2007). Another class of endogenous sRNA is ta-siRNAs, which cleaves the targets that are non-identical to them and are therefore referred as trans-acting siRNAs. ta-siRNAs are 21-nucleotide phased sRNAs that are processed from TAS genes (Chen 2009).

With the advent of next-generation sequencing technology, a large number of conserved and novel miRNAs, and siRNAs have been identified in various plant species during the last decade (Sunkar et al. 2012; Sun 2012; Jover-Gil et al. 2005). However, only a limited number of developmental roles pertaining to these sRNAs have been characterized. There are reports on functional divergence of conserved miRNAs, which could be a result of critical sequence variation in the mature miRNA and/or its complementary target sequence occurring during the coevolution of miRNAs and their targets (Barik et al. 2014, 2015).

Biogenesis of sRNAs (miRNA and ta-siRNA) is a multistep process involving various components specific for each type. Biogenesis of miRNA differs from that of ta-siRNA due to the formation of the stem loop precursor. In contrast, ta-siRNA biogenesis itself involves miRNA-mediated cleavage of TAS locus (Allen et al. 2005). A wide number of studies have been carried out in Arabidopsis thaliana to address the role of sRNAs and various other biogenesis components in plant growth and development. However, with the advent of new technologies and availability of genome sequences, orthologues of sRNA biogenesis pathway components have also been identified in rice, maize, soybean, poplar, etc. (Nagasaki et al. 2007; Chitwood et al. 2009; Husbands et al. 2009). In this review, we summarize the biogenesis and developmental roles of sRNAs, mainly miRNA and ta-siRNA in plants, and the recent advancements made in this area.

miRNA biogenesis

The biogenesis of miRNA is a multistep process involving its transcription, processing and modification and loading onto RISC (Fig. 1a). Similar to protein-coding genes, MIRNA genes are also transcribed by RNA polymerase II, which generates primary transcripts of miRNAs (pri-miRNAs) containing both 5′ cap and 3′ poly A tail (Xie et al. 2005). The presence of TATA box in the promoter of miRNA genes suggests that transcriptional regulation of miRNAs is similar to that of protein-coding genes (Zhao et al. 2013; Barik et al. 2014). miRNA biogenesis involves processing of primary miRNA (pri-miRNA) to precursor miRNA (pre-miRNA) by DICER-LIKE1 (DCL1) protein. DCL1 along with HYPONASTY LEAVES1 (HYL1) and SERRATE (SE) further processes pre-miRNA to produce 21 nt miRNA/miRNA* duplex (Vazquez et al. 2004). In vitro assays showed that HYL1 and DCL1 are required for accurate excision of pri-miRNA during miRNA biogenesis (Dong et al. 2008). Mutation in any of these three genes results in drastic reduction in the level of mature miRNAs also due to an impaired processing the amount of pri-miRNA is increased (Yang et al. 2006; Han et al. 2004; Vazquez et al. 2004). Next step in miRNA/miRNA* processing is the methylation of a duplex on 2´OH of the 3´ terminal nucleotides by HUA ENHANCER1 (HEN1), a miRNA methyltransferase which acts in a sequence–independent and structure-dependent manner (Yu et al. 2005). The final step in miRNA biogenesis is the loading of one miRNA (21–24 nt) strand from the duplex on ARGONAUTE 1 (AGO1), forming miRNA–RISC. Since AGO1 has endonucleolytic activity, it cleaves mRNA–miRNA duplex nearly in the middle of the strand (Baumberger and Baulcombe 2005; Qi et al. 2005).
Fig. 1

Biogenesis of sRNAs. a Biogenesis of miRNA. RNA Pol II transcribes a MIRNA gene into a capped and polyadenylated pri-miRNA. pri-miRNA is further processed into a stem–loop (hairpin) precursor known as pre-miRNA by DCL1 protein in Arabidopsis. The pre-miRNA is later processed into a duplex of miRNA–miRNA* by DCL1. During miRNA biogenesis, DCL1 works along with HYL1, which is a double-stranded RNA binding protein. Another protein, HEN1 methylate the 2′ OH of the 3′ terminal nucleotides of miRNA–miRNA* duplex. One strand of the miRNA–miRNA* duplex is loaded into an AGO1 having miRISC. b Biogenesis of ta-siRNA. ta-siRNA biogenesis starts from TAS1, TAS2, TAS3 and TAS4 loci. At the TAS1, TAS2, TAS4 loci, long noncoding transcripts are cleaved by miR173 or miR828 loaded AGO1. The 3′ cleaved products are bounded by SGS3/LBL1, which stabilizes ssRNA and prevents its degradation. ssRNA is copied into the dsRNA by RDR6/SHL2. The dsRNA is further processed into ~ 22 nt long siRNAs by the activity of DCL4/SHO1. At TAS3 locus, miR390 along with AGO7/SHO2/RGD2 recognizes noncoding transcripts at 5′ and 3′ site. miR390/AGO7 complex cleaves the transcripts only at 3′ end. The 5′ cleaved products are channeled into ta-siRNA production by the activity of SGS3, RDR6, and DCL4, which targets ARF2, ARF3, and ARF4 transcripts in Arabidopsis (Chen 2009, 2012; Nagasaki et al. 2007; Nogueira and Timmermans 2007)

ta-siRNA biogenesis

In Arabidopsis, four TAS gene families namely TAS1, TAS2, TAS3, and TAS4 have been identified which are present at eight genetic loci (Allen et al. 2005; Rajagopalan et al. 2006). ta-siRNA biogenesis is initiated by the cleavage of the TAS transcripts by miRNAs and further processing involves the action of various proteins specific to ta-siRNA biogenesis (Fig. 1b). Based on the number of miRNA binding target sites, TAS families are divided into two categories: one hit and two hit. The “one hit” targets which include TAS1, TAS2 and TAS4 have only one miRNA binding site in the primary-TAS transcript, whereas “two hit” target TAS3 has two miRNA binding sites (Yoshikawa 2013). ta-siRNA is derived from 3´ and 5´ fragment after miRNA cleavage in “one hit” and “two hit” category, respectively. The polarity of fragments derived after miRNA cleavage, which generates ta-siRNA, also differs among these categories. TAS1 and TAS2 derived ta-siRNAs are generated by the activity of 22-nt miR173-AGO1 complex and they target members of penta-tricopeptide repeats (Montgomery et al. 2008b; Felippes and Weigel 2009), whereas in case of TAS3, the 21-nt miR390 uniquely associates with AGO7 leading to the processing of precursor TAS3 and finally the formation of functional ta-siRNA. These ta-siRNAs target members of the AUXIN RESPONSE FACTORs (ARF) gene family (ARF2, ARF3, and ARF4), and therefore are known as tasiR-ARFs (Fahlgren et al. 2006; Garcia et al. 2006; Marin et al. 2010). The biogenesis of TAS4-derived ta-siRNAs requires 22-nt miR828. TAS4 targets MYB transcription factors PRODUCTION OF ANTHOCYANIN PIGMENT 1 (PAP1), PAP2 and MYB113 which regulate anthocyanin biosynthesis (Luo et al. 2012). ta-siRNA biogenesis requires SUPPRESSOR OF GENE SILENCING3 (SGS3), RNA-DEPENDENT RNA POLYMERASE6 (RDR6), AGO1, DICER LIKE4 (DCL4), HYL1, and HEN1 (Allen et al. 2005; Peragine et al. 2004; Rajagopalan et al. 2006; Vazquez et al. 2004; Yoshikawa et al. 2005). SGS3 stabilizes the single-stranded cleaved RNA transcript, and RDR6 converts it to double-stranded RNA. This double-stranded RNA is converted into 21-nt ta-siRNA by DCL4 (Gasciolli et al. 2005; Xie et al. 2005; Yoshikawa et al. 2005). One of the two strands of the phased ta-siRNA is loaded on AGO1 effector complex (Baumberger and Baulcombe 2005). The role of different sRNA biogenesis components across the various plant species is summarized in Table 1.
Table 1

Role of the small RNA biogenesis component in various species across the plant kingdom

ta-siRNA components

Mutant

Plant species

Role in plant development

References

SGS3

lbl1

Zea mays

Maize leaf polarity establishment

Dotto et al. (2014)

Ppsgs3

Physcomitrella patens

Gametophyte development

Plavskin et al. (2016)

sgs3

Arabidopsis thaliana

Vegetative phase change

Peragine et al. (2004)

RDR6

Zmrdr6

Zea mays

Maize leaf and shoot development

Petsch et al. (2015)

shl2

Oryza sativa

SAM maintenance in rice

Nagasaki et al. (2007)

rdr6

Arabidopsis thaliana

Gynoecium development, leaf development

Peragine et al. (2004)

AGO7

ago7

Arabidopsis thaliana

Defense response to virus, vegetative phase change

Montgomery et al. (2008a)

rgd2

Zea mays

Dorsiventral patterning of maize leaves

Douglas et al. (2010)

sho2

Oryza sativa

SAM maintenance in rice

Nagasaki et al. (2007)

DCL4

dcl4

Arabidopsis thaliana

Vegetative phase change

Gasciolli et al. (2005)

sho1

Oryza sativa

SAM formation during embryogenesis in rice

Nagasaki et al. (2007)

Zmdcl4

Zea mays

Maize leaf and shoot development

Petsch et al. (2015)

Ppdcl4

Physcomitrella patens

Regulate sporophyte formation

Plavskin et al. (2016)

HEN1

hen1

Arabidopsis thaliana

Leaf proximal/distal pattern formation

Chen et al. (2002)

waf1

Oryza sativa

Shoot development in rice

Abe et al. (2010)

AG01

ago1

Arabidopsis thaliana

Leaf proximal/distal pattern formation

Baumberger and Baulcombe (2005)

ago1a-d

Oryza sativa

Pleiotropic developmental phenotype

Wu et al. (2009)

Role of sRNAs in plant development

Initial genetic screening and loss of function or mis-expression analysis of various sRNA genes and their biogenesis components shed light into the developmental roles of several miRNAs and ta-siRNAs. A wide range of developmental processes are regulated by sRNAs starting from lower plants like moss to the higher plants like Arabidopsis, Oryza sativa and Zea mays (Nagasaki et al. 2007; Cho et al. 2012; Marin et al. 2010; Yoon et al. 2010; Talmor-Neiman et al. 2006; Juarez et al. 2004b). The roles of miRNA and ta-siRNA in various plant developmental processes are summarized in Table 1.

sRNAs in seed development and germination

Seed is an evolutionary adaptation of land plants which facilitates dispersal and allows germination when the environmental conditions turn favorable (Willmann et al. 2011; Das et al. 2015). Seeds contain miniature new plants as dormant embryos. Studies have shown that miRNA and ta-siRNA pathways regulate seed germination in Arabidopsis (Sarkar Das et al. 2018). Mutation in sRNA biogenesis pathway genes, such as DCL1 leads to severe embryogenesis and seed development defects (Willmann et al. 2011; Das et al. 2015). Overexpression of miR160 is reported to cause hyposensitivity to abscisic acid (ABA) during the seed germination process (Liu et al. 2007). miR160 is known to target ARF10/16/17 and mutation in ARF10 leads to defect in seed development (Liu et al. 2007). Both miR156 and miR172 are the master regulators of phase transition and seed germination in plants (Li and Zhang 2015). It was reported that several miRNAs, such as miR165/166, miR160, miR159, miR395, miR417 and miR402 play important roles in seed development, maturation and seed germination processes (Das et al. 2015). Overexpression of miR402 enhances seed germination in Arabidopsis under salt, osmotic and cold stress conditions (Kim et al. 2010a). Under abiotic stress conditions, miR395 acts as both positive as well as negative regulator of seed germination. miR417 is found to negatively regulate seed germination under salt stress condition in Arabidopsis (Jung and Kang 2007; Kim et al. 2010b). The short tandem target mimicry of miR165/166 (STTM165/166) plants is hypersensitive to ABA during seed germination and early seedling development (Yan et al. 2016). Auxin homeostasis is vital for embryo development and is mediated by the action of miR165/166, miR167, miR164, miR158 and miR160 (Martin et al. 2010). The role of different miRNAs in seed development is shown in Fig. 2.
Fig. 2

miRNA-mediated regulation of embryogenesis and seed development, and seed germination. Several miRNAs have been implicated in the embryonic/seed development in plants. Some miRNAs regulate the embryonic development from pre-globular to mature embryonic stages by regulating the various stages of the development in Arabidopsis. In addition to the embryonic development, miRNAs also regulate the event of seed growth and germination by regulating the expression of various key target genes, which leads to the formation of the mature seedling. Arrows indicate the regulation. miRNAs involved in embryogenesis and seed development are mentioned in purple color, miRNAs involved in seed germination  are mentioned in green color and common miRNAs are mentioned in red color

sRNAs in root development

Several sRNAs are known to regulate root growth and patterning by targeting different transcription factors or genes involved in root development (Fig. 3a) (Gautam et al. 2017). For example, miR160 is essential for root growth, branching by negative regulation of its target genes ARF10, ARF16 and ARF17 (Wang et al. 2005; Mallory et al. 2005). miR164 regulates lateral root (LR) emergence and branching through the regulation of NAM/ATAF/CUC1 (NAC1) transcription factor (Guo et al. 2005). ARF6 and ARF8 are positive regulators of adventitious root growth and both are under tight regulation by miR167 (Gutierrez et al. 2009). miR393 cleaves TRANSPORT INHIBITOR RESPONSE1 (TIR1) and AUXIN SIGNALING F-BOX2 (AFB2) subsequently regulating LR growth (Chen et al. 2012). miR165/166 and its target genes are involved in vasculature differentiation and root growth (Carlsbecker et al. 2010). A recent study shows that miR165/166 regulates root growth through phytohormonal crosstalk (Singh et al. 2017). Like morphogens in animals, some mobile sRNAs also form a gradient and define cell fate boundaries in plants (Benkovics and Timmermans 2014). In Arabidopsis root, SHORT-ROOT (SHR) protein moves from stele to endodermis and activates SCARECROW (SCR) expression. In situ hybridization and miRNA sensor experiments have shown that SCR and SHR transcriptionally activate the expression of MIR165a and MIR166b in the endodermis. Mature miR165/166 moves radially from endodermis in both inward and outward direction and degrades Class III HOMEODOMAIN-LEUCINE ZIPPER (HDZIP III) transcripts resulting in differential accumulation of target mRNA in the root vasculature (Fig. 3b) (Carlsbecker et al. 2010).
Fig. 3

Role of sRNAs in root development. a sRNA-mediated regulation of root development in dicots and monocots. Different root types were shown in dicots (approximately 7-day-old) as, adventitious root (AR), LR, and PR and in monocots (approximately 14-day-old) as crown root (CR), seminal root (SR), PR and LR. The model shows the role of important miRNAs in different root types in monocot and dicot. Dashed lines indicate the potential effect of sRNAs on monocot root development. b sRNA movement during xylem cell patterning. Diagrammatic representation of the miR165/166 movement which is a prerequisite for differentiation of xylem cell. The figure represents a transverse section of young Arabidopsis root. Cell layers shown in the figure are an outer blue color for endodermis, inner light green for pericycle, yellow are procambial cells, dark green cells are sieve elements, brown cells are companion cells, purple cells are metaxylem and orange is for protoxylem. A mechanistic model for root vascular cell patterning suggested in the figure shows that SHR moves from pericycle to endodermis and forms dimer with SCR. SCR-SHR dimer in endodermis stimulates miR165/166 and later moves towards the stele region and targets HDZIP IIIs. The differential gradient of miR165/166 and HDZIP IIIs inside the stele region regulates xylem cell differentiation

In Arabidopsis, miR396 has been found to regulate stem cell niche (SCN) by targeting GROWTH RESPONSE FACTORS (GRFs) and thus regulate cell division (Bazin et al. 2013; Rodriguez et al. 2015). Recently, it has been reported that miR171 cleaves HAIRY MERISTEM (HAM) (Llave et al. 2002; Engstrom et al. 2011). Ectopic expression of miR171 affects primary root (PR) length, a mutation in HAMs causes defective quiescent centre (QC) and stunted root growth (Wang et al. 2010; Zhou et al. 2015). In Arabidopsis, miR847 is important for LR development by regulating the expression of INDOLE ACETIC ACID 28 (IAA28). Downregulation of IAA28 leads to increase LR number (Wang and Guo 2015). miR408 and miR528 target CUPREDOXIN and subsequently regulate root cap formation, LR development and root elongation (Liu et al. 2012).

Components of the ta-siRNA pathway are also known to play an important role in Arabidopsis root development (Fig. 3a). Studies show that tasiR-ARF regulates LR growth and development by negatively regulating ARF3 and ARF4 (Marin et al. 2010; Yoon et al. 2010). Overexpression of TAS3a results in increased LR length, whereas mutation in TAS3a leads to reduced LR length (Marin et al. 2010). It was found that targets of the tasiR-ARF, ARF3 and ARF4 regulate the expression of auxin-induced miR390 by feedback mechanism (Yoon et al. 2010). Thus, LR growth is regulated by the quantitative action of miR390, ta-siRNA, auxin and ARFs (Marin et al. 2010). LR density has also been reported to be reduced in rdr6-11 and arf4-2 mutants (Yoon et al. 2010). Additionally, a negative feedback loop between tasiR-ARF and ARF4, mediates the spatiotemporal expression of ARF4 (Yoon et al. 2010). miR390 senses the auxin maxima and TAS3 derived ta-siRNA inhibits expression of ARF4, mediating the LR growth in Arabidopsis (Yoon et al. 2010; Marin et al. 2010). The miR390 expression is restricted to the lower parts and edges of the LR primordium except at the center during LR development (Marin et al. 2010). miR390 activity is detected in the whole primordium indicating that miR390 acts in a non-cell autonomous manner and moves to few neighboring cells in the root (Marin et al. 2010). A few miRNAs are hypothesized to regulate root development in monocot plants (Fig. 3a).

sRNAs in shoot apical meristem (SAM) maintenance

SAM is responsible for giving rise to the aerial organs of the plant. SAM contains pluripotent stem cells, which are maintained in the undifferentiated state by a negative feedback loop activity between WUSCHEL (WUS) and CLAVATA3 (CLV3) (Aichinger et al. 2012). SAM maintenance is controlled by the activity of several genes and sRNAs (Fig. 4). The effectiveness of WUS-dependent stem cell signaling can be increased by ZWILLE/ARGONAUTE10 (AGO10), which competes with AGO1 to bind miR165/166 and maintains the transcript level of HDZIP III genes (Aichinger et al. 2012; Zhu et al. 2011) (Fig. 4a).
Fig. 4

sRNA-mediated regulation of SAM development in plants. a Mobile sRNAs regulates embryonic SAM development. SAM is divided into central zone (CZ) and peripheral zone (PZ), which represents central zone and peripheral zone, respectively. CZ of SAM is further divided into three layers L1–L3. miR394 expresses in the L1 layer of SAM and targets LCR gene in the L3 layer. Movement of miR394 in the L3 layer is important for proper SAM development and specification. LCR in L3 layer further regulates WUS and maintains SCN. Regulation of WUS and CLV3 is also essential for proper specification of SAM. Upregulation of HDZIP IIIs due to AGO10 mediated decoying of miR165/166 leads to proper maintenance of SAM (Zhu et al. 2011; Knauer et al. 2013; Aichinger et al. 2012). b Mobile miR390 and miR166 regulates post-embryonic SAM development. The balanced activity of miR166 and target HDZIP IIIs, as well as tasiR-ARF and target ARFs is crucial for SAM maintenance in plants. Model here shows the accumulation of miR166 and ARF3 in the abaxial domain of the leaf primordia (highlighted by red color and dark blue dot, respectively), the adaxial domain is marked by the expression of target HDZIP IIIs and tasiR-ARF (highlighted by green color and orange dot, respectively). There exists a gradient of HDZIP IIIs in developing SAM (highlighted by the diffused accumulation of HDZIP III in green color). miR390 and TAS3a accumulates in the adaxial and SAM region (highlighted by magenta and light green dots, respectively). P1 indicates the first primordia and P0 indicates the incipient leaf primordia. ‘Ad’ indicate the adaxial surface, ‘Ab’ indicate the abaxial surface

miR394 regulates SAM maintenance in Arabidopsis by targeting and downregulating the expression of LEAF CURLING RESPONSIVENESS (LCR) gene which affects WUS–CLV3 pathway (Fig. 4a). pMIR394B:YFP indicates its expression in the epidermal L1 layer of the SAM; however, miR394 restricts the target LCR expression in the L3 layer (Knauer et al. 2013). As evident by in situ localization, mature miR394 moves from L1 to L3 layer, where it restricts the expression domain of the target LCR and maintains shoot SCN (Knauer et al. 2013). ta-siRNA plays an important role in meristem organization in monocots. It has been shown that mutation in maize LEAFBLADELESS1 (LBL1), a homolog of SGS3 in Arabidopsis, leads to defective meristem (Nogueira et al. 2009). Further, mutation in rice RDR6/SHOOTLESS2 (SHL2), AGO7/SHOOT ORGANIZATION2 (SHO2) and DCL4/SHO1 leads to lack of SAM (Nagasaki et al. 2007). In rice, defects in SAM formation observed in shl mutants were due to the loss of expression of HDZIP IIIs gene family members (Nagasaki et al. 2007).

sRNAs in leaf development

Leaf develops from a small group of undifferentiated cells and forms defined organ having medio-lateral, proximal–distal and abaxial–adaxial symmetry. Abaxial–adaxial surfaces of leaf are opposite faces of leaf, which are meant for different functions, e.g., adaxial surface is mainly involved in photosynthesis and abaxial is in gaseous exchange (Pulido and Laufs 2010). In Arabidopsis, abaxial–adaxial polarity of leaf is also maintained by the coordinated action of sRNAs such as miR165/166, through negative regulation of HDZIP IIIs. The expression of HDZIP IIIs in adaxial surface is maintained through negative regulation of miR165/166 which is expressed at abaxial surface of leaf (Pulido and Laufs 2010).

miR394-mediated downregulation of LCR is important for regulating leaf morphology and establishing the leaf polarity (Knauer et al. 2013). Like miRNAs, ta-siRNAs such as tasiR-ARF is also hypothesized to move from adaxial L1 layer inwards and regulate dorsiventral leaf polarity in maize and Arabidopsis by restricting the expression of target ARF2/3/4 in the abaxial domain (Chitwood and Timmermans 2010). Interestingly, it is assumed that the expression of tasiR-ARF in the adaxial domain and miR165/166 in the abaxial domain form inwards gradients, which help to establish leaf polarity through downregulation of their respective targets (Chitwood and Timmermans 2010) (Fig. 4b). The formation of final leaf shape and size requires the activity of TEOSINTE BRANCHED/CYCLOIDEA/PROLIFERATING CELL FACTORS (TCPs), which are targeted by miR319. TCP expression is reduced upon miR319 overexpression resulting in increased leaf serration and altered leaf shape (Palatnik et al. 2003). It has been shown that miR396 regulates leaf shape by targeting GROWTH-REGULATING FACTORS (GRFs) (Rodriguez et al. 2010). miR396 expression is activated by TCPs suggesting that miR319 and miR396 regulate leaf shape development in a coordinated manner (Schommer et al. 2014). Another miRNA, miR164 regulates leaf serration by negatively targeting CUP-SHAPED COTYLEDON2 (CUC2) (Nikovics et al. 2006).

In maize, the roles of components of ta-siRNA pathway are implicated in establishing leaf polarity (Fig. 5). TAS3-derived ta-siRNAs require LBL1/SGS3 for the biogenesis of ta-siRNA from the TAS3 loci on the adaxial side of the incipient primordia, which guides the cleavage of the ZmARF3 transcripts (Nogueira et al. 2007; Chitwood et al. 2009; Husbands et al. 2009; Nogueira et al. 2009). lbl1 displays abaxialized leaf fate due to the complete loss of the adaxial cell identity (Kidner and Timmermans 2007, 2010; Chitwood et al. 2007, 2009; Nogueira et al. 2007; Timmermans et al. 1998). miR166 expressed at the abaxial side of the incipient primordia restricts the expression domain of HDZIP III genes on the adaxial surface (Husbands et al. 2009). The opposite activities of TAS3-derived ta-siRNAs and miR166 specify the polarity in developing maize leaves (Chitwood et al. 2007). ROLLED1 (RLD1), one of the members of HDZIP III gene family in maize, is expressed on the adaxial side of the leaf. The expression of RLD1 in adaxial domain is confined by the abaxial specific activity of miR166 (Juarez et al. 2004a). A semi-dominant Rld1-Original (Rld1-O) mutant results in increased accumulation of HDZIP III transcripts, leading to adaxialized leaf fate (Juarez et al. 2004a, b).
Fig. 5

Model illustrating the leaf polarity through ta-siRNA and miR166 in maize and Arabidopsis. Cross section of maize leaf is divided into adaxial and abaxial surfaces. On the adaxial surface, LBL1/SGS3 is required for biogenesis of tasiR-ARFs. tasiR-ARFs cleaves ZmARF3 transcripts which are accumulated on the abaxial (ab) side. ZmARF3 directly regulates the expression of miR166c, which accumulates on the abaxial surface. miR166 targets members of the HDZIP IIIs and restricts their expression on the adaxial surface of maize leaf. The opposing activities of miR166 and HDZIP IIIs regulate leaf polarity in maize and Arabidopsis (Nogueira and Timmermans 2007; Nogueira et al. 2007)

In Lotus japonicus, the role of ta-siRNA has been established in regulating leaf development. L. japonicus has a compound arrangement of the leaves, which is different from that of Arabidopsis, rice, and maize. In L. japonicus, compound leaves are arranged as five leaflets from top to bottom. Leaflets are divided into three categories such as top leaflet (TL), lateral leaflet (LL) and basal leaflet (BL). Two ta-siRNA biogenesis pathway genes have been characterized in lotus, REDUCED LEAFLET1 (REL1) and REDUCED LEAFLET3 (REL3) which are the orthologues of Arabidopsis SGS3 and AGO7, respectively (Yan et al. 2010). rel1 and rel3 mutants show altered leaf polarity and reduced number of leaflet. BL is absent in both rel1 and rel3 mutants and the leaflets are elongated and pin-shaped (Yan et al. 2010). These mutants depicted the critical role of ta-siRNA pathway in leaflet development and formation.

In Medicago truncatula, the mutation in ta-siRNA biogenesis components, SGS3 and RDR6, leads to severe developmental and physiological defects (Bustos-Sanmamed et al. 2014). M. truncatula sgs3a and rdr6.2 mutants show downwardly curled leaves with increased serration, and even lobed margin (Bustos-Sanmamed et al. 2014). The TAS3 derived ta-siRNA plays a significant role in maintenance of fruit quality and yield in Vitis vinifera. The ta-siRNAs derived from vviTAS3 generally targets ARF4/5 transcription factor, DIN1a protein, L10 (ribosomal protein), ribosomal protein S1, ferric reductase, RAD24 (a DNA damage checkpoint protein) and many other uncharacterized proteins whose functions have not been clearly identified (Zhang et al. 2012).

sRNAs in flower development and phase transition

Life cycle of a plant involves two phase transitions; juvenile to adult phase transition and adult to reproductive phase transition. The gradient of two miRNAs, miR156 and miR172, is responsible for these phase transitions (Fig. 6a). Ectopic expression of miR156 causes altered vegetative phase transition and delayed flowering (Yu et al. 2010; Xing et al. 2013). Flower development is regulated by a network of genes and sRNAs. In both dicots and monocots, miR156, miR159, miR171, miR172 and miR396 are known to regulate floral identity and timing (Fig. 6b) (Smoczynska and Szweykowska-Kulinska 2016). miR156/157 negatively regulates SQUAMOSA-PROMOTER BINDING PROTEIN LIKE (SPLs) which subsequently regulate floral timing (Gandikota et al. 2007). Arabidopsis genome encodes 17 SPL genes of which 11 are post-transcriptionally targeted by miR156 (Rhoades et al. 2002). SPL3, SPL4 and SPL5 regulate vegetative phase to reproductive phase transition (Schwab et al. 2005; Wang et al. 2008; Wu and Poethig 2006). miR159 controls flowering time by regulating floral meristem identity gene LEAFY (LFY) by negative regulation of gibberellic acid (GA)-specific transcriptional regulator GAMYB-related proteins (MYB33, MYB65, and MYB101) (Blazquez et al. 1998). These proteins mediate the GA-induced regulation of LFY. Overexpression of miR159 causes reduced expression of LFY and delays flowering time (Achard et al. 2004). In Arabidopsis, miR171a is expressed in the inflorescence and regulates SCARECROW LIKE (SCL) SCL6-III and SCL6-IV (Nikovics et al. 2006). In maize, miR172 negatively regulates AP2-like gene GLOSSY15 (GL15) in turn regulating juvenile to adult shoot transition (Lauter et al. 2005). miR172 stimulates flowering and is involved in the fate determination of floral meristem by downregulation of its target AP2 and a small group of AP2-like genes; including TARGET OF EAT1 (TOE1), TOE2, TOE3, SCHLAFMUTZE (SMZ), and SCHNARCHZAPFEN (SNZ) (Chen 2004; Aukerman and Sakai 2003).
Fig. 6

miRNA-mediated regulation of phase transition and floral development in plants. a miR156 and miR172 are important for juvenile to adult phase transition by regulating the activity of their target genes. The cumulative action of the selected miRNAs and target genes regulate the floral development tin both dicot and monocot plants. Arrows indicate the regulation. b Regulation of floral development and identity: miR156, miR159, miR171, miR172 and miR396 regulate floral development in both monocot and dicot plants

Floral development is also regulated by miR167, which targets ARF6 and ARF8 (Nagpal et al. 2005). A resistant version of ARF6 and ARF8 causes sterility suggesting the important role of miR167 in floral development (Wu et al. 2006). Many sRNA biogenesis pathway genes are known to be involved in pollen development and a number of miRNAs have been localized to viable pollen cells (Grant-Downton et al. 2013). miRNAs regulated male reproduction have been found to be overlapping among Arabidopsis and rice suggesting their conserved function during pollen development. miR156, miR160, miR167 and miR173 are found to be present in pollen tissue (He et al. 2015).

Conclusions and perspectives

Several characterized sRNAs play important roles in modulating the development of seed, root shoot, leaf, and floral organs in both monocot and dicot plants. Mutations in the sRNA biogenesis components lead to the pleiotropic developmental defects in plants, which underlines the functional importance of sRNAs (miRNAs and ta-siRNA) in shaping the various aspects of plant development. Components of sRNA biogenesis pathway and their function appear to be quite conserved among diverse groups of plants. Many sRNAs, such as miR165/166, miR167, miR156, etc. have been implicated in development of both shoot and root. Some miRNAs/ta-siRNAs are also having partially conserved role in shoot and leaf patterning between monocot and dicot plants. Although next-generation sequencing (NGS) approach has identified huge number of sRNAs, only a handful of them have been characterized for their function, even in popular model plants, like Arabidopsis and rice. Advanced technology, like laser capture microdissection (LCM) may be applied to identify miRNAs and targets that are enriched in specific developmental tissue of plants (Gautam et al. 2016; Gautam and Sarkar 2015). Often the multigenic origin of a sRNA species and multiple targets makes the functional study of sRNA a difficult one. More exhaustive effort is required to understand the function of many novel sRNAs. As discussed above, some level of functional diversification of miRNA or their targets is predicted to be there, due to their co-evolution. Functional characterization of these sRNAs and their targets will shed light on the evolutionary conservation/divergence of sRNA-mediated regulation of plant development among diverse plant species. Developmental regulation by crosstalk of sRNAs with hormonal signaling, epigenetic regulation is poorly understood and an interesting area to be explored. Besides, traditional loss/gain-of-functional approaches, genome editing of sRNA or target loci may help to foster their functional characterization for role in plant development and physiological responses.

Author contribution statement

AS, VG, AKS, designed the outline of the article, composed the manuscript and figures. SS, SV, SD, SM, VM, and AKS provided scientific feedback and critical comments and revised the content. All the authors read and approved the manuscript.

Notes

Acknowledgements

AS, VG, SS acknowledge CSIR-India for funding and financial support. VM acknowledges DBT-India for funding. SSD acknowledges Women Scientist-A (Wos-A) fellowship from Department of Science and Technology, India (WOS-A/LS-1276/2014). SV and SM thank Department of Science and Technology—Science and Engineering Research Board (DST-SERB) for National-Post Doctoral Fellowship (N-PDF). AKS acknowledges NIPGR for funding and internal grants. We sincerely apologize to authors whose interesting work could not be cited due to space constraint.

References

  1. Abe M, Yoshikawa T, Nosaka M, Sakakibara H, Sato Y, Nagato Y, Itoh J (2010) WAVY LEAF1, an ortholog of Arabidopsis HEN1, regulates shoot development by maintaining microRNA and trans-acting small interfering RNA accumulation in rice. Plant Physiol 154(3):1335–1346.  https://doi.org/10.1104/pp.110.160234 PubMedPubMedCentralGoogle Scholar
  2. Achard P, Herr A, Baulcombe DC, Harberd NP (2004) Modulation of floral development by a gibberellin-regulated microRNA. Development 131(14):3357–3365.  https://doi.org/10.1242/dev.01206 PubMedGoogle Scholar
  3. Aichinger E, Kornet N, Friedrich T, Laux T (2012) Plant stem cell niches. Annu Rev Plant Biol 63:615–636.  https://doi.org/10.1146/annurev-arplant-042811-105555 PubMedGoogle Scholar
  4. Allen E, Xie Z, Gustafson AM, Carrington JC (2005) microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121(2):207–221.  https://doi.org/10.1016/j.cell.2005.04.004 PubMedGoogle Scholar
  5. Aukerman MJ, Sakai H (2003) Regulation of flowering time and floral organ identity by a MicroRNA and its APETALA2-like target genes. Plant Cell 15(11):2730–2741.  https://doi.org/10.1105/tpc.016238 PubMedPubMedCentralGoogle Scholar
  6. Axtell MJ (2013) Classification and comparison of small RNAs from plants. Annu Rev Plant Biol 64:137–159.  https://doi.org/10.1146/annurev-arplant-050312-120043 PubMedGoogle Scholar
  7. Barik S, SarkarDas S, Singh A, Gautam V, Kumar P, Majee M, Sarkar AK (2014) Phylogenetic analysis reveals conservation and diversification of micro RNA166 genes among diverse plant species. Genomics 103(1):114–121.  https://doi.org/10.1016/j.ygeno.2013.11.004 PubMedGoogle Scholar
  8. Barik S, Kumar A, Sarkar Das S, Yadav S, Gautam V, Singh A, Singh S, Sarkar AK (2015) Coevolution pattern and functional conservation or divergence of miR167s and their targets across diverse plant species. Sci Rep 5:14611.  https://doi.org/10.1038/srep14611 PubMedPubMedCentralGoogle Scholar
  9. Baumberger N, Baulcombe DC (2005) Arabidopsis ARGONAUTE1 is an RNA Slicer that selectively recruits microRNAs and short interfering RNAs. Proc Natl Acad Sci USA 102(33):11928–11933.  https://doi.org/10.1073/pnas.0505461102 PubMedGoogle Scholar
  10. Bazin J, Khan GA, Combier JP, Bustos-Sanmamed P, Debernardi JM, Rodriguez R, Sorin C, Palatnik J, Hartmann C, Crespi M, Lelandais-Briere C (2013) miR396 affects mycorrhization and root meristem activity in the legume Medicago truncatula. Plant J 74(6):920–934.  https://doi.org/10.1111/tpj.12178 PubMedGoogle Scholar
  11. Benkovics AH, Timmermans MC (2014) Developmental patterning by gradients of mobile small RNAs. Curr Opin Genet Dev 27:83–91.  https://doi.org/10.1016/j.gde.2014.04.004 PubMedGoogle Scholar
  12. Blazquez MA, Green R, Nilsson O, Sussman MR, Weigel D (1998) Gibberellins promote flowering of arabidopsis by activating the LEAFY promoter. Plant Cell 10(5):791–800PubMedPubMedCentralGoogle Scholar
  13. Bustos-Sanmamed P, Hudik E, Laffont C, Reynes C, Sallet E, Wen J, Mysore KS, Camproux AC, Hartmann C, Gouzy J, Frugier F, Crespi M, Lelandais-Briere C (2014) A Medicago truncatula rdr6 allele impairs transgene silencing and endogenous phased siRNA production but not development. Plant Biotechnol J 12(9):1308–1318.  https://doi.org/10.1111/pbi.12230 PubMedGoogle Scholar
  14. Carlsbecker A, Lee JY, Roberts CJ, Dettmer J, Lehesranta S, Zhou J, Lindgren O, Moreno-Risueno MA, Vaten A, Thitamadee S, Campilho A, Sebastian J, Bowman JL, Helariutta Y, Benfey PN (2010) Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate. Nature 465(7296):316–321.  https://doi.org/10.1038/nature08977 PubMedPubMedCentralGoogle Scholar
  15. Chen X (2004) A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303(5666):2022–2025.  https://doi.org/10.1126/science.1088060 PubMedGoogle Scholar
  16. Chen X (2009) Small RNAs and their roles in plant development. Annu Rev Cell Dev Biol 25:21–44.  https://doi.org/10.1146/annurev.cellbio.042308.113417 PubMedPubMedCentralGoogle Scholar
  17. Chen X (2012) Small RNAs in development—insights from plants. Curr Opin Genet Dev 22(4):361–367.  https://doi.org/10.1016/j.gde.2012.04.004 PubMedPubMedCentralGoogle Scholar
  18. Chen X, Liu J, Cheng Y, Jia D (2002) HEN1 functions pleiotropically in Arabidopsis development and acts in C function in the flower. Development 129(5):1085–1094PubMedPubMedCentralGoogle Scholar
  19. Chen H, Li Z, Xiong L (2012) A plant microRNA regulates the adaptation of roots to drought stress. FEBS Lett 586(12):1742–1747.  https://doi.org/10.1016/j.febslet.2012.05.013 PubMedGoogle Scholar
  20. Chitwood DH, Timmermans MC (2010) Small RNAs are on the move. Nature 467(7314):415–419.  https://doi.org/10.1038/nature09351 PubMedGoogle Scholar
  21. Chitwood DH, Guo M, Nogueira FT, Timmermans MC (2007) Establishing leaf polarity: the role of small RNAs and positional signals in the shoot apex. Development 134(5):813–823.  https://doi.org/10.1242/dev.000497 PubMedGoogle Scholar
  22. Chitwood DH, Nogueira FT, Howell MD, Montgomery TA, Carrington JC, Timmermans MC (2009) Pattern formation via small RNA mobility. Genes Dev 23(5):549–554.  https://doi.org/10.1101/gad.1770009 PubMedPubMedCentralGoogle Scholar
  23. Cho SH, Coruh C, Axtell MJ (2012) miR156 and miR390 regulate tasiRNA accumulation and developmental timing in Physcomitrella patens. Plant Cell 24(12):4837–4849.  https://doi.org/10.1105/tpc.112.103176 PubMedPubMedCentralGoogle Scholar
  24. Das SS, Karmakar P, Nandi AK, Sanan-Mishra N (2015) Small RNA mediated regulation of seed germination. Front Plant Sci 6:828.  https://doi.org/10.3389/fpls.2015.00828 PubMedPubMedCentralGoogle Scholar
  25. Dong Z, Han MH, Fedoroff N (2008) The RNA-binding proteins HYL1 and SE promote accurate in vitro processing of pri-miRNA by DCL1. Proc Natl Acad Sci USA 105(29):9970–9975.  https://doi.org/10.1073/pnas.0803356105 PubMedGoogle Scholar
  26. Dotto MC, Petsch KA, Aukerman MJ, Beatty M, Hammell M, Timmermans MC (2014) Genome-wide analysis of leafbladeless1-regulated and phased small RNAs underscores the importance of the TAS3 ta-siRNA pathway to maize development. PLoS Genet 10(12):e1004826.  https://doi.org/10.1371/journal.pgen.1004826 PubMedPubMedCentralGoogle Scholar
  27. Douglas RN, Wiley D, Sarkar A, Springer N, Timmermans MC, Scanlon MJ (2010) ragged seedling2 encodes an ARGONAUTE7-like protein required for mediolateral expansion, but not dorsiventrality, of maize leaves. Plant Cell 22(5):1441–1451.  https://doi.org/10.1105/tpc.109.071613 PubMedPubMedCentralGoogle Scholar
  28. Engstrom EM, Andersen CM, Gumulak-Smith J, Hu J, Orlova E, Sozzani R, Bowman JL (2011) Arabidopsis homologs of the petunia hairy meristem gene are required for maintenance of shoot and root indeterminacy. Plant Physiol 155(2):735–750.  https://doi.org/10.1104/pp.110.168757 PubMedGoogle Scholar
  29. Fahlgren N, Montgomery TA, Howell MD, Allen E, Dvorak SK, Alexander AL, Carrington JC (2006) Regulation of AUXIN RESPONSE FACTOR3 by TAS3 ta-siRNA affects developmental timing and patterning in Arabidopsis. Curr Biol 16(9):939–944.  https://doi.org/10.1016/j.cub.2006.03.065 PubMedGoogle Scholar
  30. Felippes FF, Weigel D (2009) Triggering the formation of tasiRNAs in Arabidopsis thaliana: the role of microRNA miR173. EMBO Rep 10(3):264–270.  https://doi.org/10.1038/embor.2008.247 PubMedPubMedCentralGoogle Scholar
  31. Gandikota M, Birkenbihl RP, Hohmann S, Cardon GH, Saedler H, Huijser P (2007) The miRNA156/157 recognition element in the 3′ UTR of the Arabidopsis SBP box gene SPL3 prevents early flowering by translational inhibition in seedlings. Plant J 49(4):683–693.  https://doi.org/10.1111/j.1365-313X.2006.02983.x PubMedGoogle Scholar
  32. Garcia D, Collier SA, Byrne ME, Martienssen RA (2006) Specification of leaf polarity in Arabidopsis via the trans-acting siRNA pathway. Curr Biol 16(9):933–938.  https://doi.org/10.1016/j.cub.2006.03.064 PubMedGoogle Scholar
  33. Gasciolli V, Mallory AC, Bartel DP, Vaucheret H (2005) Partially redundant functions of Arabidopsis DICER-like enzymes and a role for DCL4 in producing trans-acting siRNAs. Curr Biol 15(16):1494–1500.  https://doi.org/10.1016/j.cub.2005.07.024 PubMedGoogle Scholar
  34. Gautam V, Sarkar AK (2015) Laser assisted microdissection, an efficient technique to understand tissue specific gene expression patterns and functional genomics in plants. Mol Biotechnol 57(4):299–308.  https://doi.org/10.1007/s12033-014-9824-3 PubMedGoogle Scholar
  35. Gautam V, Singh A, Singh S, Sarkar AK (2016) An efficient LCM-based method for tissue specific expression analysis of genes and miRNAs. Sci Rep 6:21577.  https://doi.org/10.1038/srep21577 PubMedPubMedCentralGoogle Scholar
  36. Gautam V, Singh A, Verma S, Kumar A, Kumar P, Mahima Singh S, Mishra V, Sarkar AK (2017) Role of miRNAs in root development of model plant Arabidopsis thaliana. Indian J Plant Physiol 22(4):382–392.  https://doi.org/10.1007/s40502-017-0334-8 Google Scholar
  37. Grant-Downton R, Kourmpetli S, Hafidh S, Khatab H, Le Trionnaire G, Dickinson H, Twell D (2013) Artificial microRNAs reveal cell-specific differences in small RNA activity in pollen. Curr Biol 23(14):R599–601.  https://doi.org/10.1016/j.cub.2013.05.055 PubMedGoogle Scholar
  38. Guo HS, Xie Q, Fei JF, Chua NH (2005) MicroRNA directs mRNA cleavage of the transcription factor NAC1 to downregulate auxin signals for arabidopsis lateral root development. Plant Cell 17(5):1376–1386.  https://doi.org/10.1105/tpc.105.030841 PubMedPubMedCentralGoogle Scholar
  39. Gutierrez L, Bussell JD, Pacurar DI, Schwambach J, Pacurar M, Bellini C (2009) Phenotypic plasticity of adventitious rooting in Arabidopsis is controlled by complex regulation of AUXIN RESPONSE FACTOR transcripts and microRNA abundance. Plant Cell 21(10):3119–3132.  https://doi.org/10.1105/tpc.108.064758 PubMedPubMedCentralGoogle Scholar
  40. Han MH, Goud S, Song L, Fedoroff N (2004) The Arabidopsis double-stranded RNA-binding protein HYL1 plays a role in microRNA-mediated gene regulation. Proc Natl Acad Sci USA 101(4):1093–1098.  https://doi.org/10.1073/pnas.0307969100 PubMedGoogle Scholar
  41. He H, Yang T, Wu W, Zheng B (2015) Small RNAs in pollen. Sci China Life Sci 58(3):246–252.  https://doi.org/10.1007/s11427-015-4800-0 PubMedGoogle Scholar
  42. Husbands AY, Chitwood DH, Plavskin Y, Timmermans MC (2009) Signals and prepatterns: new insights into organ polarity in plants. Genes Dev 23(17):1986–1997.  https://doi.org/10.1101/gad.1819909 PubMedPubMedCentralGoogle Scholar
  43. Jover-Gil S, Candela H, Ponce MR (2005) Plant microRNAs and development. Int J Dev Biol 49(5–6):733–744.  https://doi.org/10.1387/ijdb.052015sj PubMedGoogle Scholar
  44. Juarez MT, Kui JS, Thomas J, Heller BA, Timmermans MC (2004a) microRNA-mediated repression of rolled leaf1 specifies maize leaf polarity. Nature 428(6978):84–88.  https://doi.org/10.1038/nature02363 PubMedGoogle Scholar
  45. Juarez MT, Twigg RW, Timmermans MC (2004b) Specification of adaxial cell fate during maize leaf development. Development 131(18):4533–4544.  https://doi.org/10.1242/dev.01328 PubMedGoogle Scholar
  46. Jung HJ, Kang H (2007) Expression and functional analyses of microRNA417 in Arabidopsis thaliana under stress conditions. Plant Physiol Biochem 45(10–11):805–811.  https://doi.org/10.1016/j.plaphy.2007.07.015 PubMedGoogle Scholar
  47. Kidner CA, Timmermans MC (2007) Mixing and matching pathways in leaf polarity. Curr Opin Plant Biol 10(1):13–20.  https://doi.org/10.1016/j.pbi.2006.11.013 PubMedGoogle Scholar
  48. Kidner CA, Timmermans MC (2010) Signaling sides adaxial-abaxial patterning in leaves. Curr Top Dev Biol 91:141–168.  https://doi.org/10.1016/S0070-2153(10)91005-3 PubMedGoogle Scholar
  49. Kim JY, Kwak KJ, Jung HJ, Lee HJ, Kang H (2010a) MicroRNA402 affects seed germination of Arabidopsis thaliana under stress conditions via targeting DEMETER-LIKE Protein3 mRNA. Plant Cell Physiol 51(6):1079–1083.  https://doi.org/10.1093/pcp/pcq072 PubMedGoogle Scholar
  50. Kim JY, Lee HJ, Jung HJ, Maruyama K, Suzuki N, Kang H (2010b) Overexpression of microRNA395c or 395e affects differently the seed germination of Arabidopsis thaliana under stress conditions. Planta 232(6):1447–1454.  https://doi.org/10.1007/s00425-010-1267-x PubMedGoogle Scholar
  51. Knauer S, Holt Anna L, Rubio-Somoza I, Tucker Elise J, Hinze A, Pisch M, Javelle M, Timmermans Marja C, Tucker Matthew R, Laux T (2013) A protodermal miR394 signal defines a region of stem cell competence in the arabidopsis shoot meristem. Dev Cell 24(2):125–132.  https://doi.org/10.1016/j.devcel.2012.12.009 PubMedGoogle Scholar
  52. Lauter N, Kampani A, Carlson S, Goebel M, Moose SP (2005) microRNA172 down-regulates glossy15 to promote vegetative phase change in maize. Proc Natl Acad Sci USA 102(26):9412–9417.  https://doi.org/10.1073/pnas.0503927102 PubMedGoogle Scholar
  53. Li C, Zhang B (2015) MicroRNAs in control of plant development. J Cell Physiol.  https://doi.org/10.1002/jcp.25125 Google Scholar
  54. Lim LP, Lau NC, Weinstein EG, Abdelhakim A, Yekta S, Rhoades MW, Burge CB, Bartel DP (2003) The microRNAs of Caenorhabditis elegans. Genes Dev 17(8):991–1008.  https://doi.org/10.1101/gad.1074403 PubMedPubMedCentralGoogle Scholar
  55. Liu PP, Montgomery TA, Fahlgren N, Kasschau KD, Nonogaki H, Carrington JC (2007) Repression of AUXIN RESPONSE FACTOR10 by microRNA160 is critical for seed germination and post-germination stages. Plant J 52(1):133–146.  https://doi.org/10.1111/j.1365-313X.2007.03218.x PubMedGoogle Scholar
  56. Liu Z, Kumari S, Zhang L, Zheng Y, Ware D (2012) Characterization of miRNAs in response to short-term waterlogging in three inbred lines of Zea mays. PLoS ONE 7(6):e39786.  https://doi.org/10.1371/journal.pone.0039786 PubMedPubMedCentralGoogle Scholar
  57. Llave C, Xie Z, Kasschau KD, Carrington JC (2002) Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science 297(5589):2053–2056.  https://doi.org/10.1126/science.1076311 PubMedGoogle Scholar
  58. Luo Q-J, Mittal A, Jia F, Rock CD (2012) An autoregulatory feedback loop involving PAP1 and TAS4 in response to sugars in Arabidopsis. Plant Mol Biol 80(1):117–129.  https://doi.org/10.1007/s11103-011-9778-9 PubMedGoogle Scholar
  59. Mallory AC, Bartel DP, Bartel B (2005) MicroRNA-directed regulation of Arabidopsis AUXIN RESPONSE FACTOR17 is essential for proper development and modulates expression of early auxin response genes. Plant Cell 17(5):1360–1375.  https://doi.org/10.1105/tpc.105.031716 PubMedPubMedCentralGoogle Scholar
  60. Marin E, Jouannet V, Herz A, Lokerse AS, Weijers D, Vaucheret H, Nussaume L, Crespi MD, Maizel A (2010) miR390, Arabidopsis TAS3 tasiRNAs, and their AUXIN RESPONSE FACTOR targets define an autoregulatory network quantitatively regulating lateral root growth. Plant Cell 22(4):1104–1117.  https://doi.org/10.1105/tpc.109.072553 PubMedPubMedCentralGoogle Scholar
  61. Martin RC, Liu PP, Goloviznina NA, Nonogaki H (2010) microRNA, seeds, and Darwin? diverse function of miRNA in seed biology and plant responses to stress. J Exp Bot 61(9):2229–2234.  https://doi.org/10.1093/jxb/erq063 PubMedGoogle Scholar
  62. Molnar A, Schwach F, Studholme DJ, Thuenemann EC, Baulcombe DC (2007) miRNAs control gene expression in the single-cell alga Chlamydomonas reinhardtii. Nature 447(7148):1126–1129.  https://doi.org/10.1038/nature05903 PubMedGoogle Scholar
  63. Montgomery TA, Howell MD, Cuperus JT, Li D, Hansen JE, Alexander AL, Chapman EJ, Fahlgren N, Allen E, Carrington JC (2008a) Specificity of ARGONAUTE7-miR390 interaction and dual functionality in TAS3 trans-acting siRNA formation. Cell 133(1):128–141.  https://doi.org/10.1016/j.cell.2008.02.033 PubMedGoogle Scholar
  64. Montgomery TA, Yoo SJ, Fahlgren N, Gilbert SD, Howell MD, Sullivan CM, Alexander A, Nguyen G, Allen E, Ahn JH, Carrington JC (2008b) AGO1-miR173 complex initiates phased siRNA formation in plants. Proc Natl Acad Sci USA 105(51):20055–20062.  https://doi.org/10.1073/pnas.0810241105 PubMedGoogle Scholar
  65. Nagasaki H, Itoh J, Hayashi K, Hibara K, Satoh-Nagasawa N, Nosaka M, Mukouhata M, Ashikari M, Kitano H, Matsuoka M, Nagato Y, Sato Y (2007) The small interfering RNA production pathway is required for shoot meristem initiation in rice. Proc Natl Acad Sci USA 104(37):14867–14871.  https://doi.org/10.1073/pnas.0704339104 PubMedGoogle Scholar
  66. Nagpal P, Ellis CM, Weber H, Ploense SE, Barkawi LS, Guilfoyle TJ, Hagen G, Alonso JM, Cohen JD, Farmer EE, Ecker JR, Reed JW (2005) Auxin response factors ARF6 and ARF8 promote jasmonic acid production and flower maturation. Development 132(18):4107–4118.  https://doi.org/10.1242/dev.01955 PubMedGoogle Scholar
  67. Nikovics K, Blein T, Peaucelle A, Ishida T, Morin H, Aida M, Laufs P (2006) The balance between the MIR164A and CUC2 genes controls leaf margin serration in Arabidopsis. Plant Cell 18(11):2929–2945.  https://doi.org/10.1105/tpc.106.045617 PubMedPubMedCentralGoogle Scholar
  68. Nogueira F, Timmermans MC (2007) An interplay between small regulatory RNAs patterns leaves. Plant Signal Behav 2(6):519–521PubMedPubMedCentralGoogle Scholar
  69. Nogueira FT, Madi S, Chitwood DH, Juarez MT, Timmermans MC (2007) Two small regulatory RNAs establish opposing fates of a developmental axis. Genes Dev 21(7):750–755.  https://doi.org/10.1101/gad.1528607 PubMedPubMedCentralGoogle Scholar
  70. Nogueira FT, Chitwood DH, Madi S, Ohtsu K, Schnable PS, Scanlon MJ, Timmermans MC (2009) Regulation of small RNA accumulation in the maize shoot apex. PLoS Genet 5(1):e1000320.  https://doi.org/10.1371/journal.pgen.1000320 PubMedPubMedCentralGoogle Scholar
  71. Palatnik JF, Allen E, Wu X, Schommer C, Schwab R, Carrington JC, Weigel D (2003) Control of leaf morphogenesis by microRNAs. Nature 425(6955):257–263.  https://doi.org/10.1038/nature01958 PubMedGoogle Scholar
  72. Peragine A, Yoshikawa M, Wu G, Albrecht HL, Poethig RS (2004) SGS3 and SGS2/SDE1/RDR6 are required for juvenile development and the production of trans-acting siRNAs in Arabidopsis. Genes Dev 18(19):2368–2379.  https://doi.org/10.1101/gad.1231804 PubMedPubMedCentralGoogle Scholar
  73. Petsch K, Manzotti PS, Tam OH, Meeley R, Hammell M, Consonni G, Timmermans MC (2015) Novel DICER-LIKE1 siRNAs bypass the requirement for DICER-LIKE4 in maize development. Plant Cell 27(8):2163–2177.  https://doi.org/10.1105/tpc.15.00194 PubMedPubMedCentralGoogle Scholar
  74. Plavskin Y, Nagashima A, Perroud PF, Hasebe M, Quatrano RS, Atwal GS, Timmermans MC (2016) Ancient trans-acting siRNAs confer robustness and sensitivity onto the auxin response. Dev Cell 36(3):276–289.  https://doi.org/10.1016/j.devcel.2016.01.010 PubMedPubMedCentralGoogle Scholar
  75. Pulido A, Laufs P (2010) Co-ordination of developmental processes by small RNAs during leaf development. J Exp Bot 61(5):1277–1291.  https://doi.org/10.1093/jxb/erp397 PubMedGoogle Scholar
  76. Qi Y, Denli AM, Hannon GJ (2005) Biochemical specialization within Arabidopsis RNA silencing pathways. Mol Cell 19(3):421–428.  https://doi.org/10.1016/j.molcel.2005.06.014 PubMedGoogle Scholar
  77. Rajagopalan R, Vaucheret H, Trejo J, Bartel DP (2006) A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes Dev 20(24):3407–3425.  https://doi.org/10.1101/gad.1476406 PubMedPubMedCentralGoogle Scholar
  78. Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, Bartel DP (2002) Prediction of plant microRNA targets. Cell 110(4):513–520PubMedGoogle Scholar
  79. Rodriguez RE, Mecchia MA, Debernardi JM, Schommer C, Weigel D, Palatnik JF (2010) Control of cell proliferation in Arabidopsis thaliana by microRNA miR396. Development. 137(1):103–112.  https://doi.org/10.1242/dev.043067 PubMedPubMedCentralGoogle Scholar
  80. Rodriguez RE, Ercoli MF, Debernardi JM, Breakfield NW, Mecchia MA, Sabatini M, Cools T, De Veylder L, Benfey PN, Palatnik JF (2015) MicroRNA miR396 regulates the switch between stem cells and transit-amplifying cells in arabidopsis roots. Plant Cell 27(12):3354–3366.  https://doi.org/10.1105/tpc.15.00452 PubMedPubMedCentralGoogle Scholar
  81. Sarkar Das S, Yadav S, Singh A, Gautam V, Sarkar AK, Nandi AK, Karmakar P, Majee M, Sanan-Mishra N (2018) Expression dynamics of miRNAs and their targets in seed germination conditions reveals miRNA-ta-siRNA crosstalk as regulator of seed germination. Sci Rep 8(1):1233.  https://doi.org/10.1038/s41598-017-18823-8 PubMedPubMedCentralGoogle Scholar
  82. Schommer C, Debernardi JM, Bresso EG, Rodriguez RE, Palatnik JF (2014) Repression of cell proliferation by miR319-regulated TCP4. Mol Plant 7(10):1533–1544.  https://doi.org/10.1093/mp/ssu084 PubMedGoogle Scholar
  83. Schwab R, Palatnik JF, Riester M, Schommer C, Schmid M, Weigel D (2005) Specific effects of microRNAs on the plant transcriptome. Dev Cell 8(4):517–527.  https://doi.org/10.1016/j.devcel.2005.01.018 PubMedGoogle Scholar
  84. Singh A, Roy S, Singh S, Das SS, Gautam V, Yadav S, Kumar A, Singh A, Samantha S, Sarkar AK (2017) Phytohormonal crosstalk modulates the expression of miR166/165s, target Class III HD-ZIPs, and KANADI genes during root growth in Arabidopsis thaliana. Sci Rep 7(1):3408.  https://doi.org/10.1038/s41598-017-03632-w PubMedPubMedCentralGoogle Scholar
  85. Smoczynska A, Szweykowska-Kulinska Z (2016) MicroRNA-mediated regulation of flower development in grasses. Acta Biochim Pol 63(4):687–692.  https://doi.org/10.18388/abp.2016_1358 PubMedGoogle Scholar
  86. Sun G (2012) MicroRNAs and their diverse functions in plants. Plant Mol Biol 80(1):17–36.  https://doi.org/10.1007/s11103-011-9817-6 PubMedGoogle Scholar
  87. Sunkar R, Li YF, Jagadeeswaran G (2012) Functions of microRNAs in plant stress responses. Trends Plant Sci 17(4):196–203.  https://doi.org/10.1016/j.tplants.2012.01.010 PubMedGoogle Scholar
  88. Talmor-Neiman M, Stav R, Klipcan L, Buxdorf K, Baulcombe DC, Arazi T (2006) Identification of trans-acting siRNAs in moss and an RNA-dependent RNA polymerase required for their biogenesis. Plant J 48(4):511–521.  https://doi.org/10.1111/j.1365-313X.2006.02895.x PubMedGoogle Scholar
  89. Timmermans MC, Schultes NP, Jankovsky JP, Nelson T (1998) Leafbladeless1 is required for dorsoventrality of lateral organs in maize. Development 125(15):2813–2823PubMedGoogle Scholar
  90. Vazquez F, Gasciolli V, Crete P, Vaucheret H (2004) The nuclear dsRNA binding protein HYL1 is required for microRNA accumulation and plant development, but not posttranscriptional transgene silencing. Curr Biol 14(4):346–351.  https://doi.org/10.1016/j.cub.2004.01.035 PubMedGoogle Scholar
  91. Wang JJ, Guo HS (2015) Cleavage of INDOLE-3-ACETIC ACID INDUCIBLE28 mRNA by MicroRNA847 upregulates auxin signaling to modulate cell proliferation and lateral organ growth in Arabidopsis. Plant Cell 27(3):574–590.  https://doi.org/10.1105/tpc.15.00101 PubMedPubMedCentralGoogle Scholar
  92. Wang JW, Wang LJ, Mao YB, Cai WJ, Xue HW, Chen XY (2005) Control of root cap formation by MicroRNA-targeted auxin response factors in Arabidopsis. Plant Cell 17(8):2204–2216.  https://doi.org/10.1105/tpc.105.033076 PubMedPubMedCentralGoogle Scholar
  93. Wang JW, Schwab R, Czech B, Mica E, Weigel D (2008) Dual effects of miR156-targeted SPL genes and CYP78A5/KLUH on plastochron length and organ size in Arabidopsis thaliana. Plant Cell 20(5):1231–1243.  https://doi.org/10.1105/tpc.108.058180 PubMedPubMedCentralGoogle Scholar
  94. Wang L, Mai YX, Zhang YC, Luo Q, Yang HQ (2010) MicroRNA171c-targeted SCL6-II, SCL6-III, and SCL6-IV genes regulate shoot branching in Arabidopsis. Mol Plant 3:794–806PubMedGoogle Scholar
  95. Willmann MR, Endres MW, Cook RT, Gregory BD (2011) The functions of RNA-dependent RNA polymerases in Arabidopsis. Arabidopsis Book 9:e0146.  https://doi.org/10.1199/tab.0146 PubMedPubMedCentralGoogle Scholar
  96. Wu G, Poethig RS (2006) Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133(18):3539–3547.  https://doi.org/10.1242/dev.02521 PubMedPubMedCentralGoogle Scholar
  97. Wu MF, Tian Q, Reed JW (2006) Arabidopsis microRNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction. Development. 133(21):4211–4218.  https://doi.org/10.1242/dev.02602 PubMedGoogle Scholar
  98. Wu L, Zhang Q, Zhou H, Ni F, Wu X, Qi Y (2009) Rice MicroRNA effector complexes and targets. Plant Cell 21(11):3421–3435.  https://doi.org/10.1105/tpc.109.070938 PubMedPubMedCentralGoogle Scholar
  99. Xie Z, Allen E, Fahlgren N, Calamar A, Givan SA, Carrington JC (2005) Expression of Arabidopsis MIRNA genes. Plant Physiol 138(4):2145–2154.  https://doi.org/10.1104/pp.105.062943 PubMedPubMedCentralGoogle Scholar
  100. Xing S, Salinas M, Garcia-Molina A, Hohmann S, Berndtgen R, Huijser P (2013) SPL8 and miR156-targeted SPL genes redundantly regulate Arabidopsis gynoecium differential patterning. Plant J 75(4):566–577.  https://doi.org/10.1111/tpj.12221 PubMedGoogle Scholar
  101. Yan J, Cai X, Luo J, Sato S, Jiang Q, Yang J, Cao X, Hu X, Tabata S, Gresshoff PM, Luo D (2010) The REDUCED LEAFLET genes encode key components of the trans-acting small interfering RNA pathway and regulate compound leaf and flower development in Lotus japonicus. Plant Physiol 152(2):797–807.  https://doi.org/10.1104/pp.109.140947 PubMedPubMedCentralGoogle Scholar
  102. Yan J, Zhao C, Zhou J, Yang Y, Wang P, Zhu X, Tang G, Bressan RA, Zhu JK (2016) The miR165/166 mediated regulatory module plays critical roles in ABA homeostasis and response in Arabidopsis thaliana. PLoS Genet 12(11):e1006416.  https://doi.org/10.1371/journal.pgen.1006416 PubMedPubMedCentralGoogle Scholar
  103. Yang L, Liu Z, Lu F, Dong A, Huang H (2006) SERRATE is a novel nuclear regulator in primary microRNA processing in Arabidopsis. Plant J 47(6):841–850.  https://doi.org/10.1111/j.1365-313X.2006.02835.x PubMedGoogle Scholar
  104. Yoon EK, Yang JH, Lim J, Kim SH, Kim SK, Lee WS (2010) Auxin regulation of the microRNA390-dependent transacting small interfering RNA pathway in Arabidopsis lateral root development. Nucleic Acids Res 38(4):1382–1391.  https://doi.org/10.1093/nar/gkp1128 PubMedGoogle Scholar
  105. Yoshikawa M (2013) Biogenesis of trans-acting siRNAs, endogenous secondary siRNAs in plants. Genes Genetic Syst 88(2):77–84Google Scholar
  106. Yoshikawa M, Peragine A, Park MY, Poethig RS (2005) A pathway for the biogenesis of trans-acting siRNAs in Arabidopsis. Genes Dev 19(18):2164–2175.  https://doi.org/10.1101/gad.1352605 PubMedPubMedCentralGoogle Scholar
  107. Yu B, Yang Z, Li J, Minakhina S, Yang M, Padgett RW, Steward R, Chen X (2005) Methylation as a crucial step in plant microRNA biogenesis. Science 307(5711):932–935.  https://doi.org/10.1126/science.1107130 PubMedPubMedCentralGoogle Scholar
  108. Yu N, Cai WJ, Wang S, Shan CM, Wang LJ, Chen XY (2010) Temporal control of trichome distribution by microRNA156-targeted SPL genes in Arabidopsis thaliana. Plant Cell 22(7):2322–2335.  https://doi.org/10.1105/tpc.109.072579 PubMedPubMedCentralGoogle Scholar
  109. Zhang C, Li G, Wang J, Fang J (2012) Identification of trans-acting siRNAs and their regulatory cascades in grapevine. Bioinformatics 28(20):2561–2568.  https://doi.org/10.1093/bioinformatics/bts500 PubMedGoogle Scholar
  110. Zhao X, Zhang H, Li L (2013) Identification and analysis of the proximal promoters of microRNA genes in Arabidopsis. Genomics 101(3):187–194.  https://doi.org/10.1016/j.ygeno.2012.12.004 PubMedGoogle Scholar
  111. Zhou Y, Liu X, Engstrom EM, Nimchuk ZL, Pruneda-Paz JL, Tarr PT, Yan A et al (2015) Control of plant stem cell function by conserved interacting transcriptional regulators. Nature 517:377–380PubMedGoogle Scholar
  112. Zhu H, Hu F, Wang R, Zhou X, Sze SH, Liou LW, Barefoot A, Dickman M, Zhang X (2011) Arabidopsis Argonaute10 specifically sequesters miR166/165 to regulate shoot apical meristem development. Cell 145(2):242–256.  https://doi.org/10.1016/j.cell.2011.03.024 PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Archita Singh
    • 1
  • Vibhav Gautam
    • 1
  • Sharmila Singh
    • 1
  • Shabari Sarkar Das
    • 2
  • Swati Verma
    • 1
  • Vishnu Mishra
    • 1
  • Shalini Mukherjee
    • 1
  • Ananda K. Sarkar
    • 1
  1. 1.National Institute of Plant Genome ResearchNew DelhiIndia
  2. 2.International Center for Genetic Engineering and BiotechnologyNew DelhiIndia

Personalised recommendations