Improving crop nutrient efficiency through root architecture modifications

JIPB

Journal of Integrative Plant Biology

Improving crop nutrient efficiency through root architecture modifications Xinxin Li1,2, Rensen Zeng1 and Hong Liao2* 1

College of Life Sciences, Fujian Agriculture and Forestry University, Fuzhou 350002, China, 2Haixia Institute of Science and Technology, Root Biology Center, Fujian Agriculture and Forestry University, Fuzhou 350002, China.

Abstract Improving crop nutrient efficiency becomes an essential consideration for environmentally friendly and sustainable agriculture. Plant growth and development is dependent on 17 essential nutrient elements, among them, nitrogen (N) and phosphorus (P) are the two most important mineral nutrients. Hence it is not surprising that low N and/or low P availability in soils severely constrains crop growth and productivity, and thereby have become high priority targets for improving nutrient efficiency in crops. Root exploration largely determines the ability of plants to acquire

INTRODUCTION

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Keywords: Nitrogen; nutrient efficiency; phosphorus; root architecture; symbiosis Citation: Li X, Zeng R, Liao H (2016) Improving crop nutrient efficiency through root architecture modifications. J Integr Plant Biol 58: 193– 202 doi: 10.1111/jipb.12434 Edited by: Leon V Kochian, USDA-ARS, Cornell University, USA Received Aug. 21, 2015; Accepted Oct. 10, 2015 Available online on Oct. 12, 2015 at wileyonlinelibrary.com/journal/ jipb © 2015 Institute of Botany, Chinese Academy of Sciences

effective nutrient acquisition is largely dependent on the ability of root systems to explore the soil. Root architecture as often defined as the spatial configuration of the root system in growth media, and determines the 3-dimensional distribution of the different root types in the root system cross the soil profile. In recent years, considerable research has shown that variation in root system architecture plays a key role in crop nutrient efficiency (Lynch 1995). Correspondingly, root architecture also can be significantly influenced by nutrient availability, heterogeneity of nutrient supply and symbiotic microorganisms (Williamson et al. 2001; Linkohr et al. 2002; He et al. 2003; Yano and Kume 2005; Walch-Liu et al. 2006; Ahokas et al. 2007; Wang et al. 2011; Wu et al. 2012). Recently, there have been an increasing number of published studies on the genetic, molecular and physiological regulation for root architecture as related to plant nutrient efficiency. A number of genes have been identified in Arabidopsis (Mlodzi
nska et al. 2015), maize (Li et al. 2011; Lin et al. 2013), rice (Wu and Wang 2008) and soybean (Guo et al. 2011), which are involved in changing root architecture to facilitate enhanced nutrient acquisition. Additionally, regulators including transcription factors (Devaiah et al. 2007; Miura et al. 2011; Dai et al. 2012), proteins (Araya et al. 2014) and miRNAs (Meng et al. 2010; Vidal et al. 2010) have also been demonstrated to participate in regulatory networks linking March 2016 | Volume 58 | Issue 3 | 193–202

Free Access

Plants require at least 17 essential nutrients for growth and development. Among them, nitrogen (N) and phosphorus (P) are the most frequently required mineral macronutrients, and are primarily taken up from soils by roots. Low N and/or low P availability in the soil severely limits plant growth and productivity in both production agricultural settings and natural environments (Gojon et al. 2009). In order to feed the expanding population, famers tend to supply excessive N/P fertilizers, which not only increases agricultural input but also becomes one of the main causes of air and water pollution (Choudhury and Kennedy 2005; Choudhury et al. 2007). Therefore, developing crops with superior nutrient efficiency becomes an essential consideration for environmentally friendly and sustainable agriculture. The plant root system is obviously essential for plant growth and serves a wide range of functions, including nutrient and water acquisition, anchorage and symbiosis with beneficial microflora in soils for enhancing the efficiency of nutrient absorption (Hodge et al. 2009). Given the low and variable availability of most mineral nutrients, which for N and P are influenced by ammonia volatilization, denitrification, leaching and runoff losses of N and high rate fixation and slow diffusion of P in soils (Sample et al. 1980; Zhao et al. 2011),

Invited Expert Review

Hong Liao *Correspondence: [email protected]

mineral nutrients from soils. Therefore, root architecture, the 3-dimensional configuration of the plant’s root system in the soil, is of great importance for improving crop nutrient efficiency. Furthermore, the symbiotic associations between host plants and arbuscular mycorrhiza fungi/rhizobial bacteria, are additional important strategies to enhance nutrient acquisition. In this review, we summarize the recent advances in the current understanding of crop species control of root architecture alterations in response to nutrient availability and root/microbe symbioses, through gene or QTL regulation, which results in enhanced nutrient acquisition.

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root architecture to nutrient efficiency. With regard to genetic research in this area, quantitative trait loci (QTL) analysis is a powerful approach for understanding genetic variation and control of genetically compiled root architecture and transport traits in response to nutrient starvation. Many QTLs for root architecture in relation to N/P deficiency stress have been characterized in maize (Li et al. 2015), rice (Shimizu et al. 2004; Shimizu et al. 2008; Li et al. 2009), bean/common bean (Liao et al. 2004; Cichy et al. 2009), and soybean (Liang et al. 2010), suggesting that these putative QTLs can be used in marker-assisted breeding and facilitate the genetic improvement for N/P efficiency. It is well known that root association with arbuscular mycorrhizal fungi (AMF) enhances nutrient acquisition, particularly for diffusion limited mineral nutrients in the soil (P and micronutrients like Zn and Cu) (Bolan 1991; Cavagnaro 2008; Andrade et al. 2010). Also, the formation of symbiotic relationships with rhizobial N2 fixing bacteria is another rootmicrobe association that improves N efficiency in most leguminous plants (Jia et al. 2004; Herridge et al. 2008; Meng et al. 2015). Interestingly, some studies have demonstrated that inoculation with AMF or rhizobial bacteria significantly influences and alters root architecture, while root growth also influences the affected microorganism infection of the roots (Berta et al. 1995; Wang et al. 2011). However, little progress has been made in understanding the underlying physiological and molecular mechanisms of root architecture remodeling as related to symbiotic associations with AMF or rhizobial bacteria. Here, we highlight the recent advances on our understanding of the regulation and mechanisms facilitating plant nutrient efficiency through plant modifications in root architecture and root associations with symbiotic microbes.

CHANGES IN ROOT ARCHITECTURE FOR BETTER NUTRIENT ACQUSITION Soil exploration by plants to facilitate nutrient uptake is largely determined by root architecture. Therefore, changing root architecture is a fundamentally important strategy to enhance nutrient acquisition, especially under nutrient deficient conditions. Nitrogen is the essential constituent for many important primary and secondary organic compounds in plans, including proteins, nucleic acids and chlorophyll (Amtmann and Armengaud 2009; Xu et al. 2012). Thus N starvation is a primary constraint for plant growth and development, with subsequent significant reductions in crop yield and productivity. Plants utilize a number of different N species in rhizosphere, including ammonium, nitrate and soluble N-containing organic compounds (amino acids and peptides) (Tegeder and Rentsch 2010). In Arabidopsis, four root morphological adaptations to different levels and forms of N supply have been characterized, including local/systemic regulation of lateral root growth, inhibition of lateral root initiation under high C:N ratio conditions, and stimulation of root branching and suppression of primary root growth due to exposure to external L-glutamate (Zhang et al. 2007). In crops such as rice, wheat and maize, root responses to low N availability are mainly through enhanced root elongation and March 2016 | Volume 58 | Issue 3 | 193–202

deeper root systems to absorb primarily nitrate, which is among the most mobile mineral nutrient ions (Wang et al. 2002; Ju et al. 2015; Rasmussen et al. 2015; Yu et al. 2015). This is exemplified by the finding that maize genotypes with less crown roots but more deep roots were more effective in N absorption from low N soils (Saengwilai et al. 2014). A root architecture ideotype with deeper, vigorous lateral roots and strong responses to nitrate has been proposed for efficient N acquisition by maize in intensive cropping systems (Mi et al. 2010), and field trials supported this via demonstration that a large and deep root system underlies high N use efficiency in maize (Figure 1) (Yu et al. 2015). Along with N, P is generally considered the most limiting essential macronutrient. P is an essential component of a number of key information and energy-containing organic molecules (e.g., DNA, RNA, ATP) and membrane phospholipids, clearly delineating the importance of P to crop growth and development (Berndt and Kumar 2007). Due to the low mobility and high fixation of P in soils, plant P acquisition largely depends on root exploration in soils in order to increase spatial P availability (Niu et al. 2013). Modifying root architecture is widely documented and recognized as an important strategy for better P uptake under P deficient conditions, allowing for improved performance on low P soils. Responses of many plant species including Arabidopsis, rice and maize to P starvation are characterized by the stimulated formation and emergence of lateral roots and root hairs (Bates and Lynch 1996; Kirk and Du 1997; Gaume et al. 2001; Williamson et al. 2001). In addition, it has been found that several plant species develop special types of root architecture in response to P deficiency (Figure 1). For instance, plants from a number of families including the leguminosae and proteacae develop dense clusters of lateral roots that are termed proteoid or cluster roots. In several lupine species within the leguminacea, these roots arise from the pericycle of first order lateral roots, and these secondary lateral roots are quite short, with an average length of 5 mm and are densely covered with root hairs (Dinkelaker et al. 1995; Neumann et al. 2000). Members of the Proteaceae develop more complex cluster roots. For example, the shrubby tree species Hakea prostrata (Harsh hakea) develops proteoid roots with thousands of densely spaced secondary lateral roots that form a characteristic “hairbrush” shape (Lamont 1972). Species from the Cyperaceae family generate dauciform proteoid roots with remarkably dense clusters of long root hairs with the clusters having a carrot shape (Shane et al. 2005). Because the phosphate (Pi) anion is one of the least mobile mineral nutrient ions for its strong interactions with Fe and Al hydroxide moieties on the surface of clay minerals, much of the P in low P soils resides in the surface soil horizon. A study of the “applied core collection” of soybean germplasm showed that plants with shallow root architecture had better spatial framework to explore P in the P-rich topsoil, and thus had higher P efficiency and yield (Zhao et al. 2004). In addition, root architecture can also be significantly altered by micronutrient deprivation, especially responses to low iron (Fe) and boron (B). The root morphology changes induced by low Fe availability are similar to those in response to P deficiency. Under low Fe conditions, root hair formation and elongation were significantly enhanced (Lopez-Bucio et al. 2003). Primary root growth was strongly www.jipb.net

Nutrient efficiency and root architecture

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Figure 1. Schematic representation of the root architecture remodeling in response to N/P availability in soils Modifying root system architecture is one of the important strategies for plants to enhance N/P acquisition from N/P-limited soils. Plants have developed deeper root systems for efficient N acquisition, especially in response to nitrate leaching, while in response to P deficiency changes in root architecture include (i) the formation of proteoid or cluster roots that can have several different cluster shapes: Proteoid (arising from the pericycle of first order lateral roots), hairbrush shape cluster roots (develop more rootlets per centimeter length of secondary/tertiary roots where almost every pericycle cells gives rise to a rootlet); and (ii) dauciform or proliferation of shallow lateral roots for greater root growth in the topsoil where more of the P is fixed in P deficient soils.

inhibited by the absence of B supply, accompanied by enhanced production of lateral roots, and development of numerous long root hairs (Takano et al. 2006; Martin-Rejano et al. 2011; Abreu et al. 2014). However, definitive evidence that alterations in root architecture improve micronutrient acquisition efficiency has not been published.

MOLECULAR MECHANISMS OF ROOT ARCHITECTURE MODIFICATION RELATED TO NUTRIENT EFFICIENCY In recent years, findings from a number of papers have begun to identify genes involved in plant root architecture changes in response to nutrient supplies. Understanding the molecular mechanisms by which crop plants alter their root architecture in response to specific nutrients would certainly help facilitate genetic improvements in nutrient efficiency through root architecture modifications. Nitrate is a major soil N source for plants, and is mainly absorbed by roots via different nitrate transporters. In Arabidopsis, the nitrate transporter/sensor NRT1.1 participates in an auxin-mediated nitrate signaling pathway associated with modifications in root architecture, while the high affinity nitrate uptake transporter, NRT2.1, has been shown to have key dual functions with regard to nitrate uptake and coordinating lateral root growth and development with nitrate availability (Remans et al. 2006; Mounier et al. 2014). An auxin biosynthetic gene, TAR2, is also involved in low N-mediated reprogramming of root architecture in Arabidopsis (Table 1) (Ma et al. 2014), further supporting the important roles auxin plays in regulation of root architecture in response www.jipb.net

to N availability. Although evidence supporting the hypothesis that multiple signaling pathways linking soil N availability and plant N status to root architecture have been presented in the literature (Walch-Liu et al. 2005; Zhang et al. 2007; Forde 2014), only a small number of genes have been characterized to play roles in this process (Table 1). Examples include the plasma membrane proton pump, AHA2, CLE peptides and a CLV1 leucine-rich repeat receptor-like kinase in Arabidopsis, which is involved in the regulation of root growth response to N availability (Araya et al. 2014; Mlodzi
nska et al. 2015). In rice, an ubiquitin ligase, EL5, has been identified, which has been suggested to act to prevent root meristematic cell death in N-triggered changes in root formation (Mochizuki et al. 2014; Nishizawa et al. 2015). In addition, microRNAs appear to play an important role in plant responses to mineral deficiency stress. In Arabidopsis, two microRNAs, including miR167 and miR393, were found to regulate their target genes, ARF8 (for miR167) and AFB3 (miR393) to modulate root architecture alterations in response to changes in N supply (Gifford et al. 2008; Vidal et al. 2010). However, this is a new field of research and the specific roles of microRNAs in regulation of root architecture remain to be elucidated. Pi starvation signaling networks and transcriptional regulation in the plant has been widely studied, but the molecular mechanisms by which plants modify their root architecture in response to changes in both soil P and plant P status remain largely unknown. A diverse collection of genes have been shown to be involved. For example, several transcription factors (TFs) including SIZ1/YRKY75 in Arabidopsis (Devaiah et al. 2007; Miura et al. 2011), OsMYB2P-1/OsPHR2 in rice (Wu and Wang 2008; Dai et al. 2012), and ZmPTF1 in maize have been identified as playing important roles in root March 2016 | Volume 58 | Issue 3 | 193–202

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Table 1. Gene identification of root traits related to nutrient efficiency in different plant species Species

Gene/QTL

Response to nutrient deficiency

Arabidopsis

NRT1.1 NRT2.1

N N

TAR2 AHA2 CLE-CLV1

N N N

MicroRNA393/AFB3 MicroRNA167/ARF8

N N

PRD

P

SIZ1 WRKY75 PIP5K CTR1 BOR2

P P P B B

Rice

EL5

N

Maize Common bean Soybean

OsPHR2 OsMYB2P-1 PSTOL1 OsARF12 ZmPTF1 PvSPX1 GmEXPB2

P P P Fe P P P

architecture remodeling by P deficiency (Li et al. 2011). Recently, several genes have been identified and suggested to be associated with root architecture modifications to improve P efficiency. First, using transcriptomics and qRT-PCR analyses, the Arabidopsis genes PRD and PIP5K were found to be involved in the regulation of root architecture responses to Pi starvation via control primary and lateral root growth as
bal et al. 2008; well as root hair elongation (Camacho-Cristo Wada et al. 2015). Additionally, fine-scale mapping of a major P uptake efficiency QTL in rice identified the protein kinase, PSTOL1, which is associated with enhanced root growth and increased grain yield on P deficient soils (Gamuyao et al. 2012). Furthermore, overexpression of GmEXPB2, a soybean b-expansin gene, significantly promoted root elongation and subsequent increased plant growth and P uptake under low P growth conditions (Guo et al. 2011). Finally, overexpression of a common bean gene, PvSPX1, resulted in increased root P accumulation and modified morphology of transgenic bean hairy roots (Yao et al. 2014). There have been a number of publications based on QTL analysis for root architecture remodeling in response to changes in P availability, but little research has been published on root remodeling in response to low N availability (Table 1). At present, only maize and rice QTLs for N use efficiency linked to root architecture have been discovered (Obara et al. 2010; March 2016 | Volume 58 | Issue 3 | 193–202

Root traits

Reference

Root architecture Lateral root development Root architecture Root architecture Lateral root development Root architecture Lateral root development Root architecture

Mounier et al. 2014 Remans et al. 2006 Ma et al. 2014 Mlodzi
nska et al. 2015 Araya et al. 2014 Vidal et al. 2010 Gifford et al. 2008


bal et al. Camacho-Cristo 2008 Root architecture Miura et al. 2011 Root development Devaiah et al. 2007 Root hair elongation Wada et al. 2015 Root development Tabata et al. 2013 Root elongation Miwa et al. 2005 Miwa et al. 2013 Root meristems Mochizuki et al. 2014 activity Nishizawa et al. 2015 Root hair development Wu and Wang 2008 Root architecture Dai et al. 2012 Root growth Gamuyao et al. 2012 Root elongation Qi et al. 2012 Root growth Li et al. 2011 Root growth Yao et al. 2014 Root architecture Guo et al. 2011

Li et al. 2015), while a large number of QTLs for root traits related to P efficiency have been mapped in many plant species. Three major QTLs involved in the root growth response to low P have been identified in Arabidopsis (Reymond et al. 2006). QTLs for root elongation induced by P starvation have been identified in rice (Shimizu et al. 2004; Shimizu et al. 2008; Li et al. 2009), and QTLs for root hair proliferation and increased seminal/lateral root branching and length in response to P deficiency were identified in maize (Zea mays L.) (Zhu et al. 2005a, 2005b; Zhu et al. 2006). A number of P efficiency/root architecture QTLs have been identified in bean and soybean. Three clusters of QTLs linked with root architecture traits and P uptake at low P have been detected in soybean (Liang et al. 2010). In common bean, a number of QTLs for root traits associated with P efficiency have been identified (Yan et al. 2004; Beebe et al. 2006; Ochoa et al. 2006). For example, three QTLs for root architecture traits identified from plants grown in the paper pouch system were shown to be associated with P acquisition traits in field (Liao et al. 2004), suggesting that these QTLs could be used to facilitate selection and breeding for new cultivars with higher N/P efficiency. Recently, a transcriptional activator of the auxin response gene, OsARF12, was identified with the apparent function of regulating root elongation and Fe accumulation in rice www.jipb.net

Nutrient efficiency and root architecture (Qi et al. 2012). Also, the Arabidopsis B efflux transporter, BOR2, and the negative regulator of the ethylene response pathway, CTR1, were identified by two different lab groups as being involved in B-mediated root development (Miwa et al. 2005; Miwa et al. 2013; Tabata et al. 2013). However, the mechanisms underlying these genes involvement in micronutrient efficiency still need further investigation.

IMPROVING NUTRIENT EFFICIENCY VIA ROOT ARCHITECTURE CHANGES ASSOCIATED WITH SYMBIOSIS Over 80% of terrestrial plant roots can be colonized by arbuscular mycorrhizal fungi (AMF), and the established symbiosis greatly benefits plant growth due to the ability if the AM fungi extends the ability of the root system to mine and acquire especially P, Zn and other essential macro and micronutrients from soils (Marschner and Dell 1994). In the AM symbiosis, the fungal hyphae penetrate the inner cortical cells of host roots, and form well differentiated arbuscules to exchange nutrients between the AMF and the roots of the host plant (Figure 2) (Parniske 2008). The other important

Figure 2. Schematic representation of the root architecture remodeling with symbiotic associations in response to nutrient availability There are two types of root architecture remodeling involving symbiotic associations under different nutrient supplies. Type I, root associations with arbuscular mycorrhizal fungi (AMF, on the left) promote root growth with higher root dry weight, more lateral root number and more fine roots in the host plant. Type II, the plant is involved in root association with AMF also or N2 fixing rhizobial bacteria (on the right) which results in inhibited root growth with reduced total root length and root surface area. In both cases, mycorrhizal or rhizobial symbiosis can significantly enhance host plant growth by improving N/P efficiency. www.jipb.net

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symbiotic association enhancing N acquisition and involves the formation in legumes of root nodules where rhizobia to fix N2 and provide nitrogenous compounds for plant N nutrition. The initial event in this symbiosis is the exchange of chemical signals between the root and the bacteria. Subsequently, the bacteria attach to root hairs and induce root hair curling, thereby entrapping the bacterial colony, leading to formation of the N2 fixing nodule (Figure 2) (Oldroyd and Downie 2004; Oldroyd and Downie 2008). Field trials with soybean showed that a deep rooting soybean genotype had greater AMF colonization under low P conditions, and had better nodulation with high P supply than a shallow rooting genotype (Wang et al. 2011). These findings suggest that root architecture is associated with the formation of symbiotic associations between roots and AMF and/or rhizobia. There are two types of root architecture remodeling associated with AMF or rhizobial associations in response to low nutrient supply (Figure 2). Type I, AMF colonization promotes increased root growth with enhanced number and length of lateral roots, more fine roots and higher root dry weight (Berta et al. 1995; Gutjahr et al. 2009; Yao et al. 2009; Wu et al. 2011a, 2011b; Liu et al. 2014a, 2014b). Type II, root-rhizobium symbiotic associations and different crop species such as soybean infected by AMF often result in inhibited root growth with reduced total root length, root surface area and root volume (Wang et al. 2011), presumably due to the carbon costs of developing nodules maintaining N2 fixation as well as the effects of AMF as related to root architecture remodeling being plant or fungi species dependent. In addition, it has been found that the effects of the AM fungus on plant growth are quite possibly influenced by variation in root architecture. A study from rice showed that the large rather than fine lateral roots are preferentially colonized by AMF (Gutjahr et al. 2009), and taproot plants had a higher mycorrhizal colonization rate than fibrous root plants (Yang et al. 2015). These findings suggest that taproot plant species might be more amenable for mycorrhiza colonization than fibrous root plants. Legume species inoculated with rhizobia also modify their root architecture, producing less roots that are shorter compared to non-inoculated plants (Figure 2). A possible explanation for this response is that nodules compete for carbohydrates with host roots, as nodulation and N2 fixation consume substantial amounts of carbohydrates and nutrients (Reich et al. 2006; Aleman et al. 2010). Therefore, better root growth with optimal mineral nutrient supply during nodulation might facilitate better nodule development, which in turn could result in improved yield. Several genes involved in AMF colonization have been shown to also regulate root growth on the host plants as summarized in Table 2. An example is the MAMI gene, which is phylogenetically related to the family of GARP transcription factors, and links root development, AMF symbiosis and P availability in Lotus japonicas (Volpe et al. 2013). Relatively more genes have been found that appear to be involved in regulation of both nodulation and root architecture remodeling in legumes. For instance, LjHAR1 in Lotus japonicas and SIN1 in common bean play essential roles in both root and nodule development (Buzas and Gresshoff 2007; Battaglia et al. 2014). Moreover, a number of genes including LATD (Bright et al. March 2016 | Volume 58 | Issue 3 | 193–202

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Table 2. Gene identification of root traits as related to mycorrhizal or rhizobial symbiosis for improving nutrient efficiency in different plant species Species

Symbiosis

Genes/QTLs

Root traits

Reference

Lotus japonicus

AMF Nodulation Nodulation

MAMI gene LjHAR1 MicroRNA160 MicroRNA166 LATD SUNN Cell division cycle16 CEP1 LATD/NIP

Root development Root development Root growth Root development Root development Root elongation Lateral root number Lateral root number Root architecture

CRA2 NOOT/COCH SIN1 GmEXPB2

Root architecture Root growth Lateral root growth Root architecture

Volpe et al. 2013 Buzas and Gresshoff 2007 Bustos-Sanmamed et al. 2013 Boualem et al. 2008 Bright et al. 2005 Schnabel et al. 2005 Kuppusamy et al. 2009 Imin et al. 2013 Harris and Dickstein 2010 Yendrek et al. 2010 Huault et al. 2014 Couzigou et al. 2012 Battaglia et al. 2014 Li et al. unpublished

Medicago truncatula

Common bean Soybean

2005), SUNN (Schnabel et al. 2005), LATD/NIP (Harris and Dickstein 2010; Yendrek et al. 2010), NOOT/COCH (Couzigou et al. 2012), microRNAs (miRNA160/166) (Boualem et al. 2008; Bustos-Sanmamed et al. 2013), and genes encoding cell cycle proteins (cell division cycle 16/CEP1/CRA2) (Kuppusamy et al. 2009; Imin et al. 2013; Huault et al. 2014) were identified in Medicago truncatula as genes with function in the growth and development of both roots and nodules. A significant positive relationship was also found between nodule establishment and root system growth through QTL analysis in pea (Bourion et al. 2010). More recently, it was found that the soybean cell wall protein, GmEXPB2, is involved in modification of root architecture and regulation of nodulation. Overexpression of GmEXPB2 in transgenic soybean plants resulted in longer roots with a larger root hair zone and denser root hairs, which significantly increased the frequency of rhizobial bacterial attachments to root hairs. This in turn resulted in increases in nodule number, weight and plant N/P content (Li et al. unpublished) (Figure 2). These results have great implications for breeding for improved crop N/P efficiency and productivity through simultaneously modifying root architecture and symbiotic associations.

OUTLOOK AND PERSPECTIVES Modifying root architecture is one of the major strategies for plant adaptation to nutrient deficiencies in soils (Wang et al. 2010). Recent progress has been made in understanding the molecular and physiological mechanisms underlying root architecture remodeling for better nutrient acquisition. However, there is much more to be discovered before being able to translate these findings to improve nutrient efficiency in crops via breeding for root traits. Molecular genetics analyses based on QTL and genomewide association studies may provide the links between the information obtained from fundamental research and the breeding of new crop varieties with better nutrient efficiency through root trait selection. Although many QTLs encoding March 2016 | Volume 58 | Issue 3 | 193–202

root architecture have been mapped in different crop species, very few successful examples have been reported for using these QTLs to genetically improve nutrient efficiency in crops. Only one major QTL from rice, Pup1 (phosphorus uptake1) was identified and introgressed into several rice varieties by marker-assisted backcrossing approach, and these lines showed a dramatic increase in P acquisition efficiency and enhanced yield (Chin et al. 2011). Subsequently, the same research group mapped-based cloned the Pup1 QTL and identified the PSTOL1 (phosphorous starvation tolerance 1), a kinase that functions to increase rice root biomass and increase rice yields on low P soils. More recently, Hufnagel et al. (2014) conducted jointed linkage and candidate gene association analysis of PSTOL1 homologs in sorghum RIL and association populations phenotyped for P efficiency in the field (grain yield on low P soil) and root morphology and architecture traits in the lab. Several different sorghum PSTOL1 genes were found to be strongly associated with P efficiency and bigger root systems with longer and finer roots, and more laterals. In an associated paper (Leiser et al. 2014) the potential for using markers linked to these PSTOL genes for the molecular breeding of improved sorghum P efficiency was presented. This is based on the findings of consistent allelic effects for PSTOL1 homologs for enhanced sorghum P efficiency between two different association panels in Africa and Brazil, which underscores the relatively stable role for these PSTOL1 homologs across different genetic backgrounds and environments. Finally, multiple interval QTL mapping identified four putative maize PSTOL1 homologs that were predominantly expressed in roots and co-localized with QTLs for root morphology, biomass and P acquisition-related characters (Mukherjee et al. 2014; Azevedo et al. 2015). But it is not clear whether these PSTOL1 homologs will be useful for facilitating breeding for improved maize P efficiency. Progress is being made in molecular breeding approaches to improve nutrient efficiency and crop productivity via the use of genelinked markers for root architecture remodeling that enhances mineral nutrient acquisition efficiency; however, there is still much to be done in this research area. www.jipb.net

Nutrient efficiency and root architecture Establishing symbiotic associations between host plants and soil microorganisms such as AMF and rhizobia is another important strategy to facilitate improved nutrient efficiency (Wang et al. 2010). Roots are the site of AMF or rhizobial colonization, thus root architecture logically may play an important role in the infection rate/quality. Although some components of the root-microbe molecular mechanisms and signaling transduction in AMF or rhizobial symbiosis have been discovered, the details and many of the components in these complex regulatory networks are still not understood. Moreover, many of the principal genes responsible for these processes still need to be identified and/or characterized and understood in much more details.

ACKNOWLEDGEMENTS We apologize for not being able to cite all related publications because of space limitations. We would like to acknowledge funding from the National Natural Science Foundation of China (U1301212) and the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB15030202).

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