Bracing for sustainable agriculture: the development and function of brace roots in members of Poaceae
Ashley N. Hostetler, Rajdeep S. Khangura, Brian P. Dilkes, Erin E. Sparks
BBracing for sustainable agriculture: the development and function of brace roots in members of
Poaceae
Ashley N. Hostetler *, Rajdeep S. Khangura *, Brian P. Dilkes , and Erin E. Sparks Affiliations : Department of Plant and Soil Sciences and the Delaware Biotechnology Institute, University of Delaware, Newark, DE 19711 Department of Biochemistry, Purdue University, West Lafayette, IN 47907 *equal contribution
Corresponding Author [email protected]
Contributions
All authors contributed to the writing and editing of the manuscript ighlights ● Aerial nodal roots (brace roots) are important in plant anchorage and consequently lodging resistance ●
In a meta-analysis, more than half of the genes known to influence brace roots in maize are also characterized to alter the juvenile-to-adult phase change ●
Agriculturally important C4 crops such as maize, sorghum, sugarcane, and
Setaria develop aerial nodal roots, however, studies of the development and function remain limited
Graphical Abstract
Abstract
Optimization of crop production requires root systems to function in water uptake, nutrient use, and anchorage. In maize, two types of nodal roots–subterranean crown and aerial brace roots function in anchorage and water uptake and preferentially express multiple water and nutrient transporters. Brace root development shares genetic control with juvenile-to-adult phase change and flowering time. We present a comprehensive list of the genes known to alter brace roots and explore these as candidates for QTL studies in maize and sorghum. The limited knowledge of brace root development and function in other members of
Poaceae . This work highlights the critical knowledge gap of aerial nodal root development and function and suggests new focus areas for breeding resilient crops. ntroduction
Plant adaptation to changing environments requires the dynamic response of root systems to optimize water uptake, nutrient use, and anchorage [1–4]. Recent work highlights the importance of aerial roots in plant adaptation. Exploring the development and function of aerial roots can fill a critical knowledge gap and identify new targets for breeding resilient crops through root system optimization. The maize (
Zea mays ) aerial root system presents an ideal target for this research. The maize root system consists of different root types including embryonic primary and seminal roots that are subterranean, and postembryonic nodal roots that are both subterranean and aerial (
Figure 1 )[4–8]. Nodal roots, a type of adventitious root, develop sequentially from stem nodes rather than the embryo or other roots (i.e. lateral roots). Two classifications of nodal roots exist in maize – those initiating from subterranean stem nodes, referred to as crown roots, and those initiating from aerial stem nodes, referred to as brace roots (
Figure 1 )[4,6–8]. Typically, five stem nodes belowground create a dense rootstock of crown roots, whereas the brace roots initiate from two or three stem nodes above the soil line [9]. The number of nodes with emerged brace roots is influenced by both genotype and environment [10–12]. From a functional perspective, embryonic roots in maize provide nutritional and structural support early in seedling establishment. However, after maize plants reach the vegetative leaf 6 (V6) stage, nutritional and structural support is primarily provided by the subterranean and aerial nodal roots [4]. Aerial nodal roots were historically observed to prop (or ‘brace’) the plant in the event of lodging (crop failure). Although many nodes above the soil produce brace roots in an acropetal sequence only the first few nodes have roots that enter the soil, a trait that has recently been shown to be important for anchorage [12–14]. Optimizing the function of these roots for sustainable agriculture requires a detailed understanding of the developmental mechanisms that regulate their formation.
Nodal Root Development
Nodal roots are adventitious roots, which develop in four sequential stages: induction, initiation, emergence, and growth (
Figure 1 )[8,15]. Induction requires one or more cell types to become founder cells with the competency to divide (
Figure 1A ). This stage is poorly understood for the development of adventitious roots and open questions remain as to which cell(s) or tissue(s) initiate adventitious roots and if founder cell establishment requires dedifferentiation [8,15]. Once founder cells are established, they are competent to begin initiation. The initiation stage is when cell division leads to observable morphological changes (i.e. presence of primordia). At the end of initiation, mature root primordia are established within the stem node (
Figure 1B ). The primordia remain in this state until further signaling promotes emergence. In the emergence stage, root primordia elongate and emerge from the node (
Figure 1C ). After emergence, root growth determines the extent of the root system, including the number of nodes containing brace roots that enter the soil (
Figure 1D ). Development can be regulated at each of these stages, which may have divergent regulation based on the plant species and adventitious root type [16]. The developmental mechanisms that regulate the first two stages of development (induction and initiation) are likely shared between subterranean crown roots and aerial brace roots. Both roots re initiating from stem nodes, which are anatomically comparable. However, the regulation of emergence and growth is likely influenced by distinct environmental cues based on the subterranean or aerial environment. This divergence is supported by different anatomy for the portion of a brace root that is in the air versus the portion that has entered soil [9]. The literature often reports collective nodal root data without distinguishing subterranean or aerial roots, which has limited the discovery of distinct developmental mechanisms. In maize, nodal root development has been characterized through screening mutants for root defects. These screens have identified mutants affecting different developmental stages of adventitious root development. Loss-of-function mutants in two paralogous genes of maize, rootless concerning crown and seminal roots1 (rtcs1) and rtcs-like1 ( rtcl1 ), exhibit root development defects. Loss of the more abundantly expressed, rtcs1 inhibits seminal, crown, and brace root primordia formation, indicating a defect in founder cell establishment or cell division ( Figure 1, Table 1 )[17]. A mutant of rtcs-like1 ( rtcl1 ) has a weaker phenotype that reduces nodal root growth after emergence ( Figure 1D ) [18]. Loss of the rice ortholog of rtcs1/rtcl1, Crown rootless1 ( Crl1/Arl1 ), blocks nodal root initiation [19–21] demonstrating a shared mechanism for nodal root induction or initiation. Another recessive mutant of maize, lateral rootless1 ( lrt1 ), is defective in the formation of primordia at the first coleoptile node suggesting divergent induction or initiation mechanisms at different nodes. The lrt1 mutants form other nodal roots but these roots have reduced growth after emergence ( Figure 1D ) [22]. Additional signals are required to promote emergence. For example, overexpression of auxin regulated gene involved in organ size8 ( argos8 ) in maize blocks nodal root emergence, but does not impact primordia formation ( Figure 1C ) [13]. While other mutants that lack nodal roots have been identified, the stage of development that is inhibited has yet to be defined. Specifically, the basic helix-loop-helix (bHLH) transcription factor mutant rootless1 ( rt1 ) [23,24] and the AP2/ERF transcription factor mutant zmrap2.7 [25] have a reduced number of nodes with roots, whereas the MATE transporter mutant big embryo1 ( bige1 ) [26] has an increased number of nodes with roots ( Supplemental Table 1 ). These genes encompass hormone pathways and transcriptional regulators. For example, the expression of RTCS1 is induced by auxin [27], a plant hormone which is essential for initiation of other stem-born roots [28–37]. The absence of primordia in the rtcs1 mutant indicates that auxin is also a key regulator of nodal root induction or initiation in maize. In contrast, the accumulation of ARGOS8 inhibits ethylene signaling and reduces nodal root emergence (
Figure 1C ) [13]. These data suggest that auxin and ethylene have distinct functions during maize nodal root development. While the interplay between auxin and ethylene in adventitious root development has been previously defined [16], the exact mechanism is highly context dependent. Several transcriptional regulators have been defined by mutant analyses, however there is very little known about the molecular mechanisms of these genes in relation to nodal root development. Maize nodal roots emerge from juvenile nodes [38]. Thus, one approach to uncover the molecular mechanisms of brace root development is to consider this link to juvenility. hase Change, Flowering Time, and Brace Roots in Maize
The juvenile-to-adult and adult-to-reproductive transitions bring major morphological and physiological changes in plant development [39,40]. The juvenile-to-adult transition refers to the competence of the shoot meristem to respond to reproductive signals and the subsequent adult-to-reproductive transition is the initiation of reproductive meristem development. Although these two transition phases are well separated by time in perennial plants, in annual plants (e.g. maize) these transitions are sometimes confused because meristem competence can occur simultaneously in the presence of reproductive signals [41]. The juvenile-to-adult phase change in flowering plants is well conserved. This conservation is highlighted by regulation of gene expression through two microRNAs (miR), miR156 and miR172, and their respective mRNA targets, SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) and APETALA2-LIKE MADS (AP2-LIKE) transcription factors [42]. miR156 represses SPL genes to retain juvenile identity in Arabidopsis, maize, and multiple woody perennial species [40,43,44]. After the transition to the adult phase, SPL transcription factors promote miR172 expression, which represses AP2-LIKE transcription factors to initiate the reproductive phase [45–48]. The emergence of brace roots from juvenile nodes may be attributed to the direct function of the miR156/SPL signaling module or indirectly as an outcome of node identity. This signaling module directly controls lateral root development in Arabidopsis independent of phase change [49], and repression of miR156 in Arabidopsis hypocotyls reduced the number of adventitious roots formed after root removal [44]. The ability of miR156 to promote adventitious root formation in Arabidopsis requires the auxin-induced expression of the rtcs1/rtcl1 paralogs [50]. Collectively, these data demonstrate both a conserved function for juvenile determinants in the development of adventitious roots and a direct role for these regulators in root development.
We have curated a list of all genes with known mutant phenotypes affecting nodal roots, which we term the Identified Annotated Modulators of Brace Roots (IAMBROOT;
Table 1 and
Supplemental Table 1 ). Consistent with the roles for determinants of phase transition in adventitious root formation, 14 of the 20 IAMBROOT genes also alter the juvenile-to-adult transition. Overexpression of miR156b/c in the maize corngrass1 ( Cg1 ) mutant extends the juvenile phase and represses multiple SPLs, including teosinte glume architecture1 ( tga1 ) [43]. Transgenic knockdown of TGA1 also resulted in an increase in nodes with brace roots [51]. In addition, loss of the miR172 target zmrap2.7 , an AP2-LIKE transcription factor also known as vegetative to generative transition1 ( vgt1 ), results in reduced brace root emergence [25,52]. This indicates that the miR156 and miR172 signaling modules regulate brace root emergence. Other genes with effects on phase transition outside of the miR156 and miR172 signaling modules are also in IAMBROOT ( Table 1 and
Supplemental Table 1 ). For example, overexpression of constans constans-like timing of cab1 ( zmcct1 ), a major photoperiod response regulator, delays phase change and promotes brace root formation [53]. Loss of early phase change ( epc ) hastens the transition from juvenile-to-adult phase and results in fewer nodes with brace roots [54,55]. The gibberellic acid (GA) biosynthetic mutants, such as dwarf plant1 ( d1 ),
3, d5 , and anther ear1 ( an1 ), extend the juvenile phase and increase the number of nodes with brace roots [38]. This is consistent with the observation that the DELLA-domain transcription factors that transduce GA signals repress spl genes, which explains the extended juvenile phase in the absence of GA [56,57]. These results highlight the intricate relationship of phase change, flowering time, and plant hormones in the timing and regulation of brace root development. In addition to individual gene analyses, nodal root traits have been mapped as quantitative trait loci (QTL) in maize ( Supplemental Table 2 ). The overlap between nodal root QTL and the IAMBROOT genes identifies candidates with known function in brace root development for 34 of the 161 QTL (
Table 2; Supplemental Table 3 ). QTL affecting brace roots map to rt1 [58] and rtcl1 [59], as well as several genes known to regulate phase change, plant hormones, and flowering time. Brace root QTL overlapped with zmcct1 and zmrap2.7 [58–60], alleles of which comprise flowering time QTL in maize [61,62]. The over-representation of flowering time and phase change regulators in IAMBROOT suggests that additional candidates for brace root QTL may be found among known flowering time regulators. Therefore, we expanded upon IAMBROOT to include proposed flowering time regulators in maize from recent findings (
Supplemental Table 4 ) and compared that list to the brace root QTL (
Supplemental Table 2 ). This overlap identified 26 QTL (
Supplemental Table 5 ) that includes indeterminate1 ( id1 ), phosphatidylethanolamine-binding protein8 / zeacentroradialis8 ( pebp8/zcn8 ), delayed flowering1 ( dlf1 ), and elongated mesocotyl1 ( elm1 ), which encode bona fide flowering time QTL in maize [11,62] but have not been investigated for effects on brace root development. Direct investigation of these genes is required to determine if they are responsible for the associated QTL. The mechanistic relationship between root developmental control and shoot meristem phase transitions may be fundamental to resource allocation in angiosperms [63]. Support for this hypothesis comes from a common garden experiment using 20 divergent dry-grassland species that found that flowering time predicted the allocation of root to shoot biomass better than phylogenetic relationships [64]. The fundamental association between the roles of roots in anchorage, water uptake, nutrient use, and now flowering time confounds the genetic analysis of brace root functions and the ability to optimize them for crop adaptation. Some experiments have resulted in independent effects on brace roots and flowering time [13,14,55], and molecular identification of these independent control mechanisms is required to test the functions of brace roots while controlling for variation in flowering time. Similar constraints on hypothesis testing are presented by the overlap between the control of juvenile-to-adult transition, adventitious root formation, lateral root emergence, and flowering time control. The shared mechanisms can result in pleiotropic effects of alleles on both flowering time and root development. Future experiments investigating the effects these genetic factors on both processes are critical for progress towards the rational design of climate and stress resilient crops. Aerial Nodal Root Function
Climate and stress resilient crops must have root systems that are optimized for plant anchorage, water uptake, and nutrient use in changing environments without compromising other physiological processes. Brace roots have been named for their importance in plant anchorage, hich contributes to lodging resistance. Lodging, defined by the vertical displacement of stalks, can be a result of stem (stalk lodging) or root (root lodging) failure [65–68]. Lodging can be exacerbated by various factors, including groundwater accumulation, wind, drought, soil type, topographical variation, management practices, and plant growth stage [66,69,70]. Efforts to understand root lodging resistance in maize have identified correlations between the number of nodes containing brace roots that enter the soil and anchorage [11–13] and this function has now been demonstrated directly [14]. Beyond anchorage, brace roots are proposed to be vital for nutrient and water acquisition [9,71]. However, this assertion is based primarily on the anatomical presence of 36 or more metaxylem elements in brace roots compared to 6 metaxylem elements in the primary root and 15-18 metaxylem elements in crown roots [49]. Direct measures of water and nutrient uptake in brace roots as compared to crown roots have been limited. One study reports the hydraulic conductance of different maize root types using a pressure probe technique and includes both crown and brace roots [72]. In this study, the total hydraulic conductivity is the same for all root types, although the relative contribution of radial (across the root) to axial (up the root) conductance varied [72]. The lack of direct water and nutrient uptake measurements is likely due to the size and complexity of the root system when brace roots enter the soil. We performed a meta-analysis of the expression of nitrate transporters, ammonium transporters, and aquaporins in crown roots, brace roots in the soil, and brace roots that remain aerial from the Maize Developmental Atlas [73]. The expression of transporters varied between all three root types, but not in any one direction that would suggest increased nutrient or water uptake in any single root type (
Supplemental Figure 1 ). Although aerial brace roots may seem like an unlikely site for nutrient and water uptake since they do not enter the soil, a recent study showed that aerial brace roots may play an important role in nutrient acquisition [74]. This study showed that, in a maize landrace, diazotrophic (nitrogen-fixing) bacteria associate with the mucilage produced from aerial brace roots. The enrichment of nitrogen in this mucilage suggested that these microbial communities could contribute to the nitrogen demand of the plant [74]. Thus, aerial brace roots may also constitute an important site of nutrient and water acquisition. Additional research is necessary to fully define the relative roles of crown roots, brace roots in the soil, and aerial brace roots in nutrient and water acquisition.
Prevalence of Brace Roots in
Poaceae
The importance of brace roots for plant anchorage, water uptake, and nutrient use may be conserved in other genera. While, aerial nodal roots are present in several genera of
Poaceae (the family that includes maize), there is limited research regarding their development and function. As highlighted above, the mechanisms of nodal root induction and initiation are likely conserved, however emergence and growth differ between subterranean and aerial roots. The term “brace root” is narrowly restricted to roots that emerge above the soil and proposed function to anchor the plant. Using this definition, brace roots are present only in the
Andropogoneae and
Paniceae tribes (
Figure 2 ). Here we present the limited research that has been reported in other genera. Future comparative studies between genera will be critical to define the shared and divergent development and function of aerial nodal roots in
Poaceae . Within the
Andropogoneae tribe, the closest maize relative,
Sorghum , shared a common ancestor 12-16 million years ago (MYA) [75,76]. Although there has been scant research on sorghum brace root development, brace root formation varies in sorghum (
Supplemental Table 2 )[77,78]. For example, the parents of a sorghum recombinant inbred line (RIL) population were shown to have a dramatically different number of nodes containing brace roots - Sansui (a Chinese landrace) has 6-8 nodes containing brace roots, whereas Jiliang 2 (an elite cultivar) only contains brace roots on the node closest to the soil [77]. Two QTL located on chromosome 6 and 7 explained 7.6% and 52.5% of the phenotypic variation, respectively [77]. A similar candidate gene search for sorghum brace root QTL indicates that the locus on chromosome 6 overlaps with the flowering time regulator maturity1 [79]. Therefore, the shared control of brace roots and flowering time (
Supplemental Table 5 ) may not be unique to maize. The importance of understanding the mechanisms of nodal root development is further supported by sugarcane, which diverged from sorghum 6-9 MYA and is more closely related to sorghum than maize [80–82]. Sugarcane is primarily propagated vegetatively, which occurs when a piece of stem, termed a sett, is planted in the soil and the root system is derived from nodes only. Sugarcane shows remarkable plasticity in nodal root phenotypes, with roots that emerge from the sett showing fine, highly branched architectures, whereas the roots that emerge from the new shoot are thick and reminiscent of the nodal roots in maize and sorghum [83].
Setaria , commonly referred to as foxtail millet, is part of the
Paniceae tribe, which is sister to the
Andropogoneae.
Like sorghum, maize, and sugarcane,
Setaria also develops aerial nodal roots (
Supplemental Figure 2 ). One recent study on crown root development in
Setaria viridis , the wild relative of the domesticated
Setaria italica , showed remarkable developmental plasticity in response to water availability [84]. Specifically, plants showed an increase in the number of crown root primordia but a decrease in crown root emergence in response to water deficit [84]. This response was conserved in the domesticated Setaria italica , the domesticated maize, and the wild relatives of maize,
Zea mays ssp. mexicana and ssp. parviglumis . Setaria is an emerging model organism due to its small stature, diploid genome, and increasingly available molecular genetic resources [85–87]. Future studies in
Setaria could rapidly advance our understanding of brace root development and function and provide a foundation for comparative studies within the
Poaceae . Conclusion
Aerial nodal roots have been identified in several genera of
Poaceae . In maize, these roots are called brace roots based on their critical function in plant anchorage, but their function has been poorly defined in other genera. The developmental mechanisms defined from current studies in maize provide a critical foundation for future comparative studies. Separating the regulation of brace root traits, phase change, and flowering time is essential to optimize brace roots without compromising other physiological processes. The future of breeding resilient crops must consider dynamic responses of plant development and function to environmental stressors. Given its central function in water uptake, nutrient use, and nchorage the root system is an obvious target. Despite recent work highlighting a role in anchorage, the aerial portion of the root system has been poorly studied. Thus, it is of critical importance to explore aerial root development and function in greater detail in maize and other members of
Poaceae . Acknowledgements
We thank Lindsay Erndwein of Illustrations by LindZeaMays for illustrating the figures of this article. We thank Dr. Andrew Doust for providing images of
Setaria brace roots (
Supplemental Figure 2 ). iterature Cited
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Locus name
Gene Model (B73v4)
Root Phenotypes
Reference rootless1 (rt1)
GRMZM2G163975
Reduced number of nodal roots
Jenkins 1930
Teopod1 (Tp1)
Increase in number of brace root whorls
Poethig 1988
Teopod2 (Tp2)
Increase in number of brace root whorls
Poethig 1988
Teopod3 (Tp3)
Increase in number of brace root whorls
Poethig 1988
Hairy sheath frayed1 (Hsf1)
GRMZM2G151223
Increase in number of brace root whorls
Moose and Sisco 1994 dwarf plant1 (d1)
GRMZM2G036340
Increase in number of brace root whorls
Evans et al., 1995 dwarf plant3 (d3)
GRMZM2G093195
Increase in number of brace root whorls
Evans et al., 1995 dwarf plant5 (d5)
GRMZM2G093603
Increase in number of brace root whorls
Evans et al., 1995 anther ear1 (an1)
GRMZM2G081554
Increase in number of brace root whorls
Evans et al., 1995 lateral rootless1 (lrt1)
Shorter nodal roots at the seedling stage
Hochholdinger and Feix 1998 early phase change (epc)
Reduced number of nodal roots
Vega et al., 2002
Corngrass1 (Cg1)
GRMZM5G838324/zmaMIR156
Increase in number of brace root whorls
Chuck et al., 2007 rootless concerning crown and seminal roots1 (rtcs1)
GRMZM2G092542
No brace roots
Taramino et al., 2007 teosinte glume architecture1 (tga1) and neighbor of tga1 (not1)
GRMZM2G101511/tga1; AC233751.1_FG002/not1
Increase in number of brace root whorls
Wang et al., 2015 rtcs-like1 (rtcl1)
AC149818.2_FG009
Reduced elongation of shoot-borne crown roots
Xu et al., 2015 big embryo1 (bige1)
GRMZM2G148937
Increase in number of brace root whorls
Suzuki et al., 2015 zmcct1
GRMZM2G381691
Increase in number of brace root whorls
Stephenson et al., 2019 zmrap2.7
GRMZM2G700665
Reduced number of nodal roots
Li et al., 2019 argos8
GRMZM2G354338
Reduced number of nodal roots
Shi et al., 2019 vivaparous8 (vp8)
GRMZM2G010353
Increase in number of brace root whorls
Evans and Poethig 1997 able 2. Summary of the overlap between IAMBROOT candidate gene list and nodal root traits mapped in QTL analysis.
Candidate genes from the IAMBROOT curated list were overlaid with known nodal root QTL. QTL were compiled from Gu et al., 2016; Ku et al., 2012; and Zhang et al., 2018. A full list can be found in Supplemental Table 3.
Annotation
Candidate Gene Model (B73 RefGenV4)
Root Traits
No. of QTL
IAMBROOT References an1
Zm00001d032961
BRN
RNPL Evans et al., 1995 argos8
Zm00001d038075
BRWN
TNWN Shi et al., 2019 cct1
Zm00001d024909
BRWN
EBRWN
ARNPL
CRN
CRNPL Minow et al., 2018
CRWN RNPL TNRN TNWN d1 Zm00001d039634
BRWN
TNWN Evans et al., 1995 d5 Zm00001d002349
TNWN Evans et al., 1995 rap2
Zm00001d010987
BRWN
BRN
CRN Minow et al., 2018
CRNPL TNWN rt1 Zm00001d040186
BRN
BRWN
TNRN Jenkins 1930
TNWN rtcl1 Zm00001d048401
BRWN
EBRWN Xu et al., 2015 rtcl1
Zm00001d048401
BRN Xu et al., 2015 p8 Zm00001d034383
BRN
TNRN Evans and Poethig, 1997
TNWN ARNPL=Aerial Root Number Per Layer; BRN=Brace Root Number; BRWN=Brace Root Whorl Number; CRN=Crown Root Number; CRNPL=Crown Root Number Per Layer;
CRWN=Crown Root Whorl Number; EBRWN=Effective Brace Root Whorl Number; RNPL=Nodal Root Number Per Layer; TNRN=Total Nodal Root Number; TNWN=Total
Nodal Whorl Number igure Legends Figure 1. Molecular development of maize nodal roots.
The maize root system consists of embryonic primary (red) and seminal (green) roots. The post-embryonic roots include the lateral (white), nodal crown (blue), and nodal brace (yellow) roots. Maize nodal roots develop from stems in four sequential stages as illustrated (A-D) for brace roots: induction, initiation, emergence, and growth. (A) The induction stage requires one or more cell types to become founder cells with the competency to divide; (B) once root primordia are established in stem nodes, plants enter the initiation stage; (C) roots then emerge from stems during the emergence stage; (D) root growth is the last stage of development. Genes that affect nodal root development are listed on the right. If the impacted stage of development has been determined, the genes are listed within the respective stages. If the specific developmental stage has not been determined, the genes are listed in brackets spanning the predicted stages.
Figure 2. Phylogenetic distribution of members in the
Poaceae family.
Aerial brace roots have been observed within sugarcane (purple), sorghum (teal), maize (yellow), and
Setaria (green), all of which are members of the
Andropogoneae and
Paniceae tribes. However, with the exception of maize, the development and function of these roots have been poorly defined. upplementary Tables Supplemental Table 1. Identified Annotated Modulators of Brace Roots (IAMBROOT)
Supplemental Table 2. Summary of all the nodal root QTL detected in various maize and sorghum studies
Supplemental Table 3. Summary of the overlap between the 161 QTLs reported in maize for nodal root trait variation and IAMBROOT gene list
Supplemental Table 4. Putative candidate gene list of maize genes that influence flowering time
Supplemental Table 5. Summary of the overlap between the 161 QTLs reported in maize for nodal root trait variation and bona fide flowering QTL in maize upplemental Figures
Supplemental Figure 1. Transcriptome meta-analysis of nutrient and water transporters in maize nodal roots.
Data were mined from the Maize Developmental Atlas, considering crown roots [Crown_Roots_Node4_V7], brace roots that enter the soil [Crown_Roots_Node5_V13], and brace roots that remain aerial [Brace_Roots_Node6_V13] [73]. Although the brace that enter the soil were designated as crown roots in [73], these roots would be classified as brace roots by our definition – developing from nodes above the soil. The expression of transporters (counts per million, CPM) in brace roots was normalized by the expression in crown roots. Normalized expression values for brace roots that enter the soil and brace roots that remain aerial were converted to log2 fold change. (A) Normalized expression data for nitrate transporters (B) Normalized expression data for ammonia transporters (C) Normalized expression data for aquaporins. There is variable expression of transporters based on nodal root type. NA indicates expression was not detected in that root type.
Supplemental Figure 2. Brace root in
Setaria . Although not described in the literature,