Controlling The Root System Architecture In Rice: Impact of Genes, Phytohormones And Root Microbiota

In order to feed expanding population, new crop varieties were generated which signicantly contribute to world food security. However, the growth of these improved plants varieties relied primarily on synthetic fertilizers, which negatively affect the environment as well as human health. Plants adapt to adverse environmental changes by adopting root systems through architectural changes at the root-type and tissue-specic changes and nutrient uptake eciency. Plants adapt and operate distinct pathways at various stages of development in order to optimally establish their root systems, such as change in the expression prole of genes, changes in phytohormone level and microbiome induced Root System Architecture (RSA) modication. Many scientic studies have been carried out to understand plant response to microbial colonization and how microbes involved in RSA improvement through phytohormone level and transcriptomic changes. we provide critical new from First, we discuss new into the genetic regulation of Next, hormonal regulation of root architecture and the impact of phytohormones in crown root and root branching is discussed. Finally, we discussed the impact of root microbiota in RSA modication and summarized the current knowledge about the biochemical and central molecular mechanisms involved.


Introduction
The world's population is projected to reach up to 9 billion by the middle of the twenty-rst century (DESA, 2019). Rice is a widely eaten cereal grain that feeds nearly half of the world's population (GRiSP, 2013).
The crop yield should increase up to 40% by 2025 on existing agricultural soils under favourable and unfavourable soil and environmental conditions to feed the expanding world's population. Roots are the plant's primary organ responsible for resource uptake, anchorage and formation of the rhizosphere zone (Chen et al., 2019). In order to increase crop productivity, root system improvement may play a signi cant role. Different Root System Architecture (RSA) ideotypes are identi ed after extensive studies; these ideotypes are tailored to different soil mineral nutrient balance and water status (Duque and Villordon, 2019).
Cultivated rice varieties considerably differ in their RSA. Rice has a relatively complex root system, consisting of the embryonic primary root and seminal roots with post-embryo adventitious roots (Kitomi et al., 2018). Primary and seminal roots have vital functions throughout the seedling stage, while at root tip, OSPIN2 plays a vital role in root gravitropic reactions and deciding RSA in rice . OsARF12 is an auxin response factor regulating auxin synthesis and polar auxin transport through OsYUCCAs, OsPINs, and OsPGPs, resulting in shortened primary root length in rice plants (Qi et al., 2012). One more gene, DEEPER ROOTING 1 (DRO1), an essential gene discovered by Uga and colleagues, changed RSA by controlling the RGA. DRO1 triggers unidirectional root growth and lower root bending in response to gravity by causing cell elongation at root tip, and it is negatively regulated by auxin (Uga et al., 2013). Another signi cant gene qSOR1 (quantitative trait locus for SOIL SURFACE ROOTING 1), a DRO1, homolog showed shallower RGA, qSOR1 is also negatively regulated by auxin, primarily expressed in root columella cells, and engaged in root gravitropic reactions . A root-speci c αexpansin gene, OsEXPA8, improved RSA by lengthening primary roots, boosting lateral roots and root hair counts, and improving rice root development (Ma et al., 2013). Another expansin gene, OsEXPB2, can modify RSA and shoot length (Zou et al., 2015). A leucine-rich receptor-like kinase, OsRPK1, negatively controls rice roots development by controlling polar auxin transport (Zou et al., 2014). The SOR1 (SOIL SURFACE ROOTING 1) modi ed RSA by altering the gravitropic root response (Hanzawa et al., 2013). OsARF16 also regulates RSA by regulating auxin transport and Fe homeostasis . OsSIZ1 is concerned with RSA manipulation as mutant of ossiz1 had short primary roots and adventitious roots than wild plants . A transcription factor OsWOX4 played a pivotal role in primary root elongation by regulating auxin transport, indicating its importance in RSA modi cation of rice root system . The expression OsMYB2P-1 also correlated with RSA regulation (Dai et al., 2012).
Further, RSA was substantially modi ed due to the overexpression of OsMYB4P gene in rice (Yang et al., 2014). OsWRKYP74 conferred RSA modi cation as the transgenic plants provide better tolerance to low Pi stress through activating genes triggered by Pi starvation and modulating RSA (Dai et al., 2016). A small GTPase, OsRab6a, plays a critical role in manipulating Fe +2 absorption in rice plants by regulating physiological functions associated with the acquisition of Fe and RSA in response to Fe-de ciency (Yang and Zhang, 2016). Furthermore, in RCc3 overexpression lines, local auxin biosynthesis and polar auxin transport increased auxin accumulation in root. RCc3 generates pleiotropic phenotypes of reinforced RSA, such as expanded growth of primary roots, adventitious and lateral roots at the seedling stage . Another root growth controlling gene OsWRKY28 in uenced root growth at the seedling stage and fertility at the reproductive stage, likely by affecting jasmonic acid (JA) or other phytohormone homeostasis . The study showed that exogenous JA treatments mimicked oswrky28 mutant phenotypes with inhibited root elongation. Further studies related to root growth suggested that OsACS1 and OsACS2 are concerned with regulating RSA modi cation, transcriptional regulation of genes induced by Pi starvation, and cellular phosphorus homeostasis. The study has shown that OsACS mutants, in particular, do not encourage lateral root growth in Pi-de cient condition, displaying the motivating involvement of ethylene in lateral root production under Pi-de ciency (Lee et al., 2019). An additional study by Singh et al., 2020 suggested that OsJAZ9 modulates RSA in response to K de ciency, as OsJAZ9 over expressed plants showed shorter seminal roots with longer lateral roots .
Lateral roots (LRs) play an essential role in RSA, allowing plants to search for water and nutrients from soil e ciently. However, in monocotyledonous plants, the mechanisms that regulate the evolution of LRs are poorly understood. According to Lee and colleagues, rice gene wavy root elongation growth 1 (WEG1) is involved in the formation of more extended and thick LRs (L-type LRs) via asymmetric cell growth in the elongation region (Lee et al., 2019). Apart from identifying and characterising RSA-related genes, several QTLs were also identi ed in diversi ed rice populations that affect the root system and grain yield. The complete knowledge may directly enhance rice irrigation and fertilizer e ciency in the molecular breeding of RSA (Zhou et al., 2016). Characterization of qRDWN6XB brings a different genetic resource for the breeding of rice cultivars and a reference point for strengthened grain yield and improved RSA under low nitrogen availability (Anis et al., 2019) (Table 2).
Hormonal regulation of root architecture The key biochemical and molecular elements of the intrinsic pathways include hormones, their receptors, signalling components, and transcription factors (TFs). While related networks of environmental stimuli receptors, downstream signal transduction, and TFs are involved in extrinsic response pathways. Many environmental perception and response network components are inter-regulated by, or shared between, intrinsically and hormonally regulated to respond to external signals (Table 3).

Primary root initiation, elongation and development
In monocots, the primary root (PR) derived from the radical and established embryogenesis is the CRsbased brous root system's rst root. The maintenance and development of quiescent centre (QC), stem cell population and cell identity differentiation create the PR's RAM. Auxin is one of the most critical phytohormones involved in regulating the root system. Changes in auxin levels able to transcriptionally regulate the different set of genes involved in root development and growth through the action of auxin/indole acetic acid (AUX/IAA) and Auxin Response Factor (ARF) modules (Guilfoyle and Hagen, 2007). The ARFs recognize and bind to auxin-responsive elements (AREs) in target gene promoters, thus activating or suppressing transcription. AUX/IAA proteins negatively regulate auxin response genes under no auxin or low auxin level by binding or inactivating ARFs activity (Abel et al., 1994). AUX/IAA proteins are intended for destruction by SCFTIR E3 ubiquitin ligase complex at higher auxin concentration (Gray et al., 2001). Another study suggested that LATERAL ROOTLESS 2 (LRT2), a cyclophilin and is in control of cis/trans isomerisation of peptidylprolyl, acts on AUX/IAA proteins. LRT2 catalyzes the isomerization of the tandem proline residues of the AUX/IAA necessary for recognition by OsTIR1. Also, the association of LRT2 with OsTIR1:OsIAA11 complex is increased by auxin and required for e cient degradation of AUX/IAAs (Jing et al., 2015). Perhaps other modules of the ARF regulation include miRNAs. For instance, the miR160 family assumes to take a considerable part in improving Arabidopsis PR and LR by tweaking ARF TFs, ARF10, and ARF16, which are functionally repetitive; however, both required for root cap cell foundation and upkeep. The overexpression of miR160 in rice also led to serious root cap defects, implying equivalent regulatory pathways in monocots (Wang et al., 2005). Furthermore, rice gene SLENDER RICE (SLR) and homolog SLENDER1 (SLN1) in barley are negative GA-mediated root growth regulators that tend to be in uenced by auxin. When auxin is present, DELLA TFs are ubiquitinated and destroyed, allowing root cell division and elongation (Ikeda et al., 2001).

From initiation to elongation of CRs
Crown roots are adventitious roots speci c to monocotyledons and called nodal root or roots that grow from shoots and account for the vast majority of its brous root system. CRs can be divided into two categories: the seminal roots of embryonic CRs that evolve during embryogenesis across the coleoptile node and the primary root (radicle), and the postembryonic CRs that occur during germination and plant life (Hochholdinger and Zimmermann, 2008). All CRs (embryonic and postembryonic), together with seminal PR, may be regarded as primary order roots because they emerge from the central plant stem and not from another root like LRs.
Most of the studies regarding root development focused on PR and LR of dicots like Arabidopsis, primarily where existing understanding regarding genetic control of CRs is derived from research ndings with mutants of rice and maize or based on Arabidopsis comparative studies of PR, LR, and adventitious root. The over-regulation of phytohormone, PR, LR, CR (monocots), and adventurous (dicots) gene families appear to have been predominantly conserved root growth (Coudert et al., 2010). Consequently, the roles of the speci c genes in the developmental pathways can differ slightly. The initiation and progression of CRs are regulated by auxin-mediated signalling, equivalent to PR and LR development in Arabidopsis (Rebouillat et al., 2009).
Auxin signals are necessary for the correct division of parenchyma cells asymmetrically. Similar to LR production in Arabidopsis, cytokinins (CK) also played a secondary role in promoting CR formation by antagonising auxin-based signalling pathways. The WUSCHEL RELATED HOMEOBOX11 (WOX11) is a rice gene that encodes auxin and CK-induced transcription factor, expressed in the early Crown Root Primordia (CRP) and actively divided areas of the apical meristem (Jain et al., 2006). CR growth was inhibited in WOX11 knock out mutants, while its overexpression increased CR cell division rates, resulting in precocious CR growth. The transcription of CK and auxin-responsive genes has also been modi ed, indicating that WOX11 could have a crucial role in incorporating auxin and CK signalling to regulate cell division rates in CRP. RR2 can operate as a negative CK signalling regulator that represses the CR emergence by repressing the CR meristem's cellular proliferation (Zhao et al., 2009). The genetic and physiologic process also regulated CRP formation, and the productions of CRs in stem nodes have at least a part environmental impact (Mergemann and Sauter, 2000). Submergence induced ethylene accumulation kills epidermal cells above CRP in deepwater rice accessions, allowing CRs to emerge through the epidermis of submerged nodal branches. The development of CRP may also be regulated by auxin, as a study by Xu and co-worker suggested that OsPIN1 gene RNAi-knockdown lines resulted in the discontinued development of CRP (Xu et al., 2005).
Recent studies have shown that gibberellic acid (GA) is also involved in CRP emergence and elongation with ethylene as a synergistic regulator. Furthermore, abscisic acid (ABA) also acts as an inhibitor of both GA and ethylene signalling pathways (Steffens and Sauter, 2005). Strigolactones can play a role in CR elongation's positive regulation, potentially through modulation of auxin uid, by promoting a meristematic cell root division (Arite et al., 2012). Rice dwarf mutants had a short CR phenotype due to an apparent decrease in cell division, resulting in a narrower meristematic region, for genes involved in SL biosynthesis (SL-de cient rice mutants max3/rms5/d17, max4/rms1/d10,d27) or SL (SL insensible rice mutants max2/rms4/d3 and d14) (Arite et al., 2012). This reduced cell distribution could be due to local auxin levels in SL modulation affecting the numbers of the meristem as seen in SL de cient and SL in PRs for homologous Arabidopsis genes.

Root microbiota affects root development
The soil has an exceptionally diverse microbiome, susceptible to nutrient availability that in uences the soil properties, including moisture, pH and nutrient content. According to a report that used deep sequencing techniques, soil type has a more signi cant impact on rhizosphere microbial communities than plant genotype . This nding suggested that soil properties are important in shaping the microbial communities of the soil and rhizosphere. Besides the land type, the nature and composition of root exudates secreted by plants in the rhizosphere are likely to in uence microbial communities (Dennis et al., 2010). Root exudates comprise amino acids, carbohydrates, organic acids, phenolics, enzymes, fatty acids and avonoids (Vives-Peris et al., 2019). Thus, the plant microbial interaction depends on soil and plant type (Ishaq, 2017). According to research, plants and rhizosphere inhabiting microbes have a rich chemical communication language, which alters the microbial community structure as well as plant growth and health (van Dam et al., 2016).
Rhizosphere microorganisms impact plant growth and agriculture by stimulating root development and increasing nutrient availability in the rhizosphere. Additionally, these microbes diversely improve plant growth and development by secreting speci c chemicals that involve root growth and development. Plants exude a diverse range of photosynthate compounds in the rhizosphere through their roots. These compounds contain polysaccharides, sugars (glucose, galactose, mannose and glucuronic acid), aromatic acids, amino acids, fatty acids and aliphatic acids (Hu et al., 2018). These compounds help in plant-microbe interaction by attracting and sustaining microorganisms (Venturi and Keel, 2016). Rhizospheric microbes reinforce plants growth by nutrient solubilization, storage, and uptake; humi cation of recalcitrant organic matter (Tfaily et al., 2014); averting pathogens entry and from colonizing in plants roots (Enebe and Babalola, 2019); harmonizing host immunity via induced systemic resistance (ISR); (Bruno et al., 2020) and regulating signalling pathways (Van Wees et al., 2008). Several microbes produce extracellular enzymes like cellulases, proteases, chitinases, lipases and β-1-3 glucanases that hydrolyze a wide range of cell wall compounds, such as cellulose, chitin, hemicelluloses and protein (Lugtenberg et al., 2017). These enzymes help to improve soil fertility by releasing organics nutrients like N, P, and K into the plant rhizosphere (Doni et al., 2019).
Apart from this, several rhizospheric microorganisms can modify RSA to improve nutrient and water exploration (Vacheron et al., 2013) through distinct mechanisms. The central mechanism of microbial modulation of RSA encompasses the altering hormonal balance in plant roots either by secreting plant hormone or producing secondary metabolites interfering with hormonal pathways concerned with root development such as CK, auxin, ethylene, GA, and ABA (Ghosh et al., 2019). Microbes have been shown to in uence postembryonic root development by modifying cell division and differentiation inside the PR and root hair emergence and LR formation . The most characteristic root phenotype of plant tolerance in nutrient stress is PR growth inhibition, along with the proliferation of LRs and root hairs result in increased nutrient assimilation and improved shoot biomass. A rise in shoot biomass accompanied by an increase in PR growth or deep root system is another phenotype. Both effects are dependent on nutrient type and availability. The plant root growth is also affected by both the microbial density as well as the distance between the bacteria and plant root (Ortíz-Castro et al., 2009). One of the critical mechanisms recently studied that several microbes affect root development by cell division and differentiation mainly at two sites, i.e., meristem zone and LR formation zone . These changes affect the plants' overall RSA, usually accompanied by changes in endogenous plant responses. Because several rhizospheric microbes have been identi ed as a producer of these hormones, it is tempting to speculate that microbial hormones may directly induce root system changes. The different studies summarize in Table 4 and impact of root microbiota on RSA in rice illustrated in Figure 2.

Plant growth promoter
Phytohormone production and secretion, such as indole-3-acetic acid (IAA) by rhizospheric microbes, may also be responsible for RSA recon guration. Microbes can also alter the signals that control for root morphogenesis in plants and modulate RSA (Ortíz-Castro et al., 2009). Thus, using rhizospheric microbes promises to be a novel and environmental friendly method of improving a crop's RSA and ultimately ensuring a long-term strategy for improving crop quality and yields.

Auxin and Cytokinin
The potent regulator of plant organogenesis is the balance of auxin and CK, which regulate the root development and shapes RSA (Jing and Strader, 2019). The endogenous ratio of auxin to CK in plants may be in uenced by auxin and CK secretion by rhizospheric microbes and microbial metabolites that may interact with these hormonal pathways. To date, IAA is the most well-studied auxin produced by large number of rhizospheric microbes (Mohite, 2013). Exogenous IAA regulates a broad range of plant development and root growth; for example, low IAA levels can promote the elongation of the PR, while higher IAA levels encourage LR formation, enhances root hair formation while reduces PR growth . Microbial metabolites like 2,4-diacetyl phloroglucinol (DAPG) and nitric oxide (NO) can also stimulate RSA changes in plants by interfering with auxin synthesis pathway. DAPG is a well known natural phenolic compound found in some speci c strains of gram-negative bacteria and responsible for antimicrobial properties of Pseudomonas uorescens (Weller et al., 2007). DAPG serve as a signal molecule for plants at low concentrations, stimulates root exudation (Phillips et al., 2004) and improves root branching ). An auxin-dependent signalling pathway can be interfered by DAPG, consequently modify RSA . Similarly, inoculation of rice endophyte Phomopsisliquidambari B3 signi cantly enhanced auxin, CK, and ethylene level in rice under varying N levels . Additionally, Azospirillum brasilense has nitrite reductase activity and produces NO during root colonization which is involved in auxin signalling pathway to regulate the development of LR (Rondina et al., 2020).

Ethylene
Another important phytohormone that inhibits root elongation is ethylene. It also inhibits auxin transport, induces senescence, and abscission of different organs, all of which contribute to fruit ripening (Iqbal et al., 2017). Apart from senescence, abscission and fruit ripening, ethylene also modulates plant defence pathways (Yang et al., 2017). Rhizospheric microbes affect ethylene level in plants by degrading precursors of ethylene. Rhizosperic microbes secrete 1-aminocyclopropane-1-carboxylic acid deaminase (ACCd), which degrades ACC (immediate precursor of ethylene) into α-ketobutyrate and ammonium. Microbes used the produced ammonium as carbon and nitrogen source (Kim et al., 2020). Thus, microbial ACCd activity is thought to reduce root ethylene production by reducing the abundance of the ethylene precursor ACC (Gamalero and Glick, 2015), thereby reducing the repressive effect of ethylene on root growth.
Abscisic acid (ABA) and gibberellic acid (GA) Several reports have revealed that rhizospheric microbes produce ABA and GA, or compounds that control the concentration of these phytohormones in plants . These phytohormones, however, play distinct roles during LR development ). An endophytic bacterium, Bacillus amyloliquefaciens RWL-1, produces ABA under saline conditions, and thus inoculation with this microbe improves salinity stress tolerance in rice (Shahzad et al., 2017).
GAs, particularly GA3, in uence rice root elongation and modulate local auxin production and polar auxin transport . Gibberellins are produced by a number of microbes, including Achromobacter xylosoxidans, Acinetobacter spp., Azospirillum spp., Bacillus spp., Herbaspirillum seropedicae, Gluconobacter diazotrophicus, and Gelhizobia (Dodd et al., 2010). The application of GA in rice at amount comparable to that produced by Azospirillum endorses root growth (Bottini et al., 2004).

Modi cation of root tissue structural properties
Changes in plant gene expression caused by microbes involved in cell wall expansion or loosening will mainly cause changes in the root cell wall's ultrastructure. The endophytic microbe Azospirillum irakense induces polygalacturonase expression in roots of inoculated rice (Sekar et al., 2000). Furthermore, another study found that exogenous application of auxin improves the role of the induced polygalacturonase found in rice roots inoculated with Azospirillum irakense (Dobbelaere et al., 2002).

Impact on plant transcriptome
The rice root architecture could be improved by changing the hormonal level or gene expression of the root architecture. For instance, the up-regulation of DRO1 in a shallow-rooted rice cultivar relates to root enhancement due to improved root growth angle, with even more downward root growth and high yield under drought condition (Uga et al., 2013). Furthermore, inoculation with Rhizophagus irregularis and Acanthamoeba castellanii increased the number of lateral roots (Kreuzer et al., 2006). In comparison to the ndings of Kreuzer et al., Azospirillum lipoferum inoculation increased the root numbers, root surface area and total root length (Chamam et al., 2013). Low level of IAA induces PR elongation, whereas high concentration promoted LR development, increased root hair formation, and decreased PR length, according to previous studies (Perrig et al., 2007;Remans et al., 2008).
Microbial strains may either directly supply IAA to the host plant or modify auxin pathways in the plant by controlling auxin-responsive genes expression. For example, Klebsiella and Azospirillum transformed tryptophan into IAA, which accounted for altering rice root growth (El-Khawas and Adachi, 1999). Similarly, a study reported that isolates from rice rhizospheric able to produce IAA and in uenced rice seedlings root length (Ashrafuzzaman et al., 2009). A recent study showed that the inoculation of Bacillus altitudinis strain FD48 could modify root architecture by increasing root thickness and the number of rising LRs while reduce the root length. The IAA modulation in rice root caused by Bacillus altitudinis strain FD48 is due to variation in the expression level of the AUX/IAA gene family. An early study suggested the association of Azospirillum with the expression of plant genes, as the inoculation of Azospirillum brasilense Sp245, enhances the expression of ethylene receptors in two rice cultivars with contrasting nitrogen acquisition capacities (Vargas et al., 2012). To create a positive relationship between the plant and bacteria, all ethylene receptors can need to be accumulated. In term of endophytes, Azoarcus was found to have differential rice root colonisation (Miché et al., 2006). A mild defensive response occurred in a less compatible interaction and followed by the stimulation of proteins linked to pathogenesis and proteins sharing domains with receptors such as pathogens induced kinases, which were also stimulated by jasmonate (Miché et al., 2006). Rice roots inoculation with endophytic microbes Herbaspirillum seropedicae caused the expression of auxin and ethylene responsive genes and the repression of PBZ1 proteins and thionins associated with defence (Brusamarello-Santos et al., 2012;Shidore et al., 2012). These ndings suggested that plant defence responses can be modulated during colonization of endophytes.
Plant-associated Bacillus can change the expression level of auxin-responsive genes, modulating auxin concentration in the root and thus changing the early stages of root architecture in rice seedlings (Ambreetha et al., 2018). Further studies suggested that AM fungi, Rhizophagus irregularis causes host to develop more LRs Paszkowski and Gutjahr, 2013), which is dependent on receptor-like kinase OsCERK1, implying that the recognition of chitin oligomers is critical in AM fungal-mediated induction of LR growth in rice. Another study reported that R. Irregularis triggers plant signalling responsible for induction of LR production, involving a receptor kinase CHITIN ELICITOR RECEPTOR KINASE 1 (CERK1) in rice (Chiu and Paszkowski, 2020;Chiu et al., 2018).

Impact on plant metabolome
Microbes are capable of altering the composition and volume of metabolites in addition to in uencing root exudation. For example, when inoculated with Herbaspirillum seropedicae, rice plants showed higher amount of malate content in shoot tissues (Curzi et al., 2008). The early effect of numerous Azospirillum strains on rice root and shoot secondary metabolite pro les has been investigated in recent studies. Secondary metabolite pro ling of two rice cultivars inoculated with two different strains of Azospirillum has shown that secondary metabolite pro les have been modi ed with phenolic compounds like avonoids hydroxyl cinnamic derivatives (Chamam et al., 2013). The relatively high concentration of quaternary compounds, glycine betaine was observed in rice infected with Pseudomonas pseudoalcali (Jha et al., 2011).

Concluding remarks and future perspectives
It is not surprising, then, that rhizospheric microbes in uence rice root development. The latest evidence on the impacts of rhizospheric microbes on root development is summarised in this review. It will encourage the use of naturally growing soil microbes in order to facilitate plant growth and health while minimising herbicides and synthetic fertilisers in the eld. Future research combining the study of plant developmental biology and plant-microbe interactions will shed light on how soil microbes in uence root development. This research will assist us in better understanding these complex cross-kingdom interactions, root developmental biology, and microbial signalling. Finally, this knowledge will aid in developing sustainable plant growth-promoting technologies, which can signi cantly improve crop yield and food security. Steffens B, Sauter M (2005) Tables   Table 1. Effects of extrinsic factors in modulating root system architecture.

Condition
Impact Genes Interactions References Root system submergence Crown root primordia development SUB1 GA, ethylene (Xu et al., 2006;Fukao et al., 2011) Drought LR emergence SUB1 ABA  Low phosphate availability Auxin, CK, Ethylene, GA (Yi et al., 2005;Bari et al., 2006) High Al 3+ Inhibition of LR initiation ART1 Auxin, ethylene (Yamaji et al., 2009)  OsARF12, controlling primary root length, shortened primary root (Qi et al., 2012) OsEXPA8 lengthening primary root, boosting lateral roots and root hair counts (Ma et al., 2013) OsEXPB2 modify RSA (Zou et al., 2015) OsWOX4 primary root elongation by regulating auxin transport  OsMYB2P-1 RSA regulation (Dai et al., 2012) OsMYB4P RSA (Yang et al., 2014) OsRPK1 negatively controls the development of rice roots (Zou et al., 2014) SOR1 modify RSA by altering root gravitropic response (Hanzawa et al., 2013) OsARF16 RSA modi cation by regulating auxin transport  OsSIZ1 RSA manipulation  OsWRKYP74 RSA modi cation (Dai et al., 2016) OsRab6a architecture of the root system in response to Fe-de cient medium (Yang and Zhang, 2016) OSPIN2 plays an important role in root gravitropic reactions and in determining RSA in rice by affecting polar auxin transport at the root tip  RCc3 expanded growth of primary roots, adventitious roots and lateral roots  OsWRKY28 in uenced the root growth at the seedling stage  OsACS1