JIPB
Journal of Integrative Plant Biology
Free Access
Editorial
Root architecture Numerous research publications over the past 20 years have made it quite clear that a better understanding of the molecular and genetic basis for variation in root system architecture (RSA) will greatly aid the development of crop varieties with improved and more efficient nutrient and water acquisition under limiting conditions. In many parts of the world, especially in developing countries, food security is threatened by drought stress and poor soil fertility, which are major limitations to crop yields. These stresses are increasing in severity as climate change is resulting in more variable and extreme weather events (Pachauri and Reisinger 2007). Furthermore, due to the rising costs for fertilizer production and distribution, and increasing water scarcity, as well as the negative environmental impacts associated with overuse of fertilizers, further increases in crop yields via increased agricultural inputs are not sustainable, nor are they economically viable in many developing countries (Lynch 2007). Thus, identifying how plants control the development of RSA can have a real impact on improving agricultural food production and world food security in the 21st century. There are many ways to describe RSA and probably the simplest definition is that root architecture is the spatial configuration of the entire root system in the soil (Fitter 1987; Lynch 1995). Root architecture can be looked at as the geometric arrangement of the individual roots within a root system in the soil volume the root system occupies. The different classes of root types are often controlled by different gene networks. Via these complex networks of genes and proteins, plants can control root type, and how the different roots are positioned and oriented via regulation of root angle, rate of root growth and degree of root branching. Control of all of these traits helps determine the overall 3D root system architecture. Genetically based variation in different RSA traits within and across plant species has been clearly linked to improved water and mineral nutrient acquisition. Thus, it is important that we better understand how plants control their RSA and use this knowledge to increase crop plant yields and water/nutrient acquisition efficiency (Berntson 1994; Lynch 2011). The world is facing an impending food crisis as we have to increase food production by 70% in the next 30–40 years to feed a world population estimated to be 9.5 billion by the year 2050. Much of this population growth is occurring in developing countries which already deal with food production problems due to agriculture on predominately nutrient-poor and water-limited soils. Therefore, 21st century agriculture will depend on the breeding of crops with improved RSA as well as enhanced root health and function, to enable significantly increased crop yields using less water and fertilizers, in order for agriculture to be carried out in a more sustainable and environmentally friendly manner. With regard to the role of RSA in more efficient nutrient acquisition, much of the pioneering work involved phosphorous (P) acquisition and P efficiency (the genetically based ability of certain genotypes to maintain higher yields on low
March 2016 | Volume 58 | Issue 3 | 190–192
P soils). P is probably the most limiting mineral nutrient and it is also the least mobile mineral nutrient in the soil, as the phosphate anion can bind tightly to iron and aluminum oxides on the surface of clay minerals, and forms insoluble precipitates with calcium, and can be tied up as organic P. High soil P fixation is a particular problem in the tropics and subtropics where the highly weathered acid soils tie up most of the P in the surface horizons of the soil (Kochian et al. 2005). Thus, in order to mine this fixed P from the soil, the plant must modify its RSA to place more lateral roots into the surface soil region and then alter the rhizosphere soil around these roots to solubilize and absorb the soil P. It has long been documented that the root systems of all plant species that have been studied undergo alterations in RSA in response to P deficiency. Through the pioneering work on top soil P foraging in bean and soybean by researchers such as Jonathan Lynch of Penn State University and Hong Liao of Fujian Agriculture and Forestry University, China, it has been shown that one of the major traits of P-efficient genotypes is the generation of ageotropic lateral roots with more shallow root angles, thus positioning more lateral roots in the surface soil horizons in order to mine the P fixed in these surface soil layers (Lynch and Brown 2001; Lynch 2007; Wang et al. 2010). Furthermore, these researchers have shown it is possible to introgress this root trait into root systems, generating bean and soybean varieties that maintain higher yields on low P soils. More recently, a research team led by Sigrid Heuer of the International Rice Research Institute and Matthias Wissuwa of the Japan International Research Center for Agricultural Sciences, cloned the first P uptake efficiency gene, Pstol1 (for phosphorous-starvation tolerance 1). Pstol1 encodes a receptor kinase which functions to help increase proliferation of finer lateral roots in the P-efficient genotypes. Subsequently, via a combination of association genetics-based candidate gene analysis and high throughput digital imaging of sorghum root morphology and architecture, Hufnagel et al. (2014) showed that in sorghum, P efficiency is conditioned by several homologues of rice Pstol1 which function to increase proliferation of longer and finer sorghum lateral roots. The most mobile nutrient in the soil is also the one most needed by plants—water. Recently, Yusaku Uga and his team at National Institute of Agrobiological Science in Tsukuba, Japan, used genetic mapping to identify a major root angle quantitative trait locus (QTL) in rice, (DRO1–for Deeper rooting 1) and then cloned the DRO1 gene responsible for this QTL via fine-scale mapping (Uga et al. 2011, 2013). The DRO1 protein was annotated as an unknown protein. Uga and coworkers characterized its function in deeper rooting varieties, near isogenic lines and transgenic lines and showed it triggered deeper root angles for rice crown roots. They showed that DRO1 expression was negatively regulated by auxin and is involved in auxin redistribution in the root tip, leading to asymmetric cell expansion and downward bending of the root in response to gravity. Most importantly with
www.jipb.net
Editorial regard to crop improvement, they showed that backcross introgression of the superior DRO1 allele into shallow rooting rice varieties led to deeper rooting varieties with substantially improved shoot biomass production and grain yields in response to moderate and severe drought stress. In this JIPB special issue on root architecture, we present three invited expert reviews, one research letter and four research papers. In the review by Li et al. (2016a) entitled “Improving crop nutrient efficiency through root architecture modifications”, the authors summarize and analyze the published literature regarding the role of root system architecture in more efficient acquisition of N and P, the two most limiting mineral nutrients for crop production. The physiological and molecular regulation of changes in root architecture that enhance N and P uptake and accumulation under limiting conditions is reviewed. Then the authors look at the state of our understanding of the interplay of root architecture with the root microbiome, with a focus on the two best understood root-microbial associations, rhizobial-based N2 fixation and root-mycorhizzal symbioses. The most recently discovered plant hormone, strigalactone, is known to play roles in root development. In the review by Kapulnik and Koltai (2016) entitled “Fine-tuning by strigolactones of root response to low phosphate”, the authors show how this hormone plays a role in communication between roots and mycorhizzal fungi, especially under P-limiting conditions. It appears that strigalactones are involved in communications between the root system and root microbiome, to help facilitate the colonization of roots by P-acquiring mycorrhizae. Finally, the review by Topp et al. (2016) entitled “How can we harness quantitative genetic variation in crop root system architecture for agricultural improvement?” addresses the new technologies that are emerging and being employed to image roots and quantify root traits grown in both transparent growth media and soils. Then, the authors review the literature on mining the digital root phenotypic data to genetically map root system architecture, how to use the results to better understand the molecular basis for variation in RSA, and finally, to breed for crops with improved root traits. The five research papers deal with a range of topics, including new technologies to image and quantify root architecture traits, the development of improved genetic resources to genetically map and dissect complex RSA traits, the interplay of nutrient status, hormones, and modification of RSA for N acquisition efficiency. The research paper by Pi~ neros et al. (2016) entitled “Evolving technologies for growing, imaging, and analyzing 3D root system architecture of crop plants”, describes recent advances and improvements in a digital optical imaging platform for RSA that enables the users to grow a range of plant species in hydroponics and soil or soil-like media, and generate 3D reconstructions of RSA for quantification of root traits. The paper entitled “Genetic dissection of maize seedling root system architecture traits using an ultra-high density bin-map and a recombinant inbred line population” by Song et al. (2016) employed QTL mapping of maize RSA traits conducted in a maize recombinant inbred line population generated from two widely used maize hybrids. A number of robust RSA QTL were identified and the findings will set the stage for more detailed genetic dissection of these complex traits in lines widely used for maize breeding. www.jipb.net
191
There are three research papers in this special issue addressing different aspects of RSA and N acquisition. In the Ruffel et al. (2016) Letter to the Editor entitled “Longdistance nitrate signaling displays cytokinin dependent and independent branches”, the authors present findings indicating that certain aspects of Arabidopsis lateral root development are under the control of long-distance systemic N signaling and that cytokinins play a role in this signaling. In the research paper entitled “Use of genotype-environment interactions to elucidate the pattern of maize root plasticity to nitrogen deficiency” by Li et al. (2016b), the authors conducted QTL mapping of maize root plasticity in response to changes in N status and found that the complex genetic control of root plasticity in response to changing N nutrition has a significant GE component, but it is possible to begin separating out the genetic component of this interaction for further mapping and possible map-based breeding of improved maize root traits. In the Araya et al. (2016) paper entitled “Statistical modeling of nitrogen-dependent modulation of root system architecture in Arabidopsis thaliana”, a statistical modeling approach was developed to study the responses of RSA to changing N status. The authors are able to begin to provide the statistical framework for a better understanding of the complex dynamics of RSA in response to a changing soil environment and plant N status, in order to begin to dissect out specific root responses in a systematic manner. From the invited reviews and research papers in this special issue on root architecture, I hope the readers will get some sense of this dynamic and rapidly growing and evolving field of research on root system development and function, and the potential for translating the findings from this research into the breeding of crop species with more vigorous, nutrient-efficient and resilient root systems. Leon V. Kochian, Professor Special Issue Editor Robert W. Holley Center for Agriculture and Health, USDA-ARS, Cornell University, Ithaca, NY 14853, USA doi: 10.1111/jipb.12471 © 2016 Institute of Botany, Chinese Academy of Sciences
REFERENCES Araya T, Kubo T, von Wir en N, Takahashi H (2016) Statistical modeling of nitrogen-dependent modulation of root system architecture in Arabidopsis thaliana. J Integr Plant Biol 58: 254–265 Berntson GM (1994) Modelling root architecture: Are there tradeoffs between efficiency and potential of resource acquisition? New Phytol 127: 483–493 Fitter AH (1987) An architectural approach to the comparative ecology of plant root systems. New Phytol 106: 61–77 Hufnagel B, de Sousa SM, Assis L, Guimaraes CT, Leiser W, Azevedo GC, Negri B, Larson BG, Shaff JE, Pastina MM, Barros BA, Weltzien E, Rattunde HF, Viana JH, Clark RT, Falc~ ao A, Gazaffi R, Garcia AA, Schaffert RE, Kochian LV, Magalhaes JV (2014) Duplicate and conquer: Multiple homologs of PHOSPHORUS-STARVATION TOLERANCE1 enhance phosphorus acquisition and sorghum performance on low-phosphorus soils. Plant Physiol 166: 659–677 Kapulnik Y, Koltai H (2016) Fine-tuning by strigolactones of root response to low phosphate. J Integr Plant Biol 58: 203–212
March 2016 | Volume 58 | Issue 3 | 190–192
192
Editorial
Kochian LV, Pi~ neros MA, Hoekenga OA (2005) The physiology, genetics and molecular biology of plant aluminum resistance and toxicity. Plant Soil 274: 175–195
Evolving technologies for growing, imaging, and analyzing 3D root system architecture of crop plants. J Integr Plant Biol 58: 230–241
Li X, Zeng RS, Liao H (2016a) Improving crop nutrient efficiency through root architecture modifications. J Integr Plant Biol 58: 193–202
Ruffel S, Poitout A, Krouk G, Coruzzi GM, Lacombe B (2016) Longdistance nitrate signaling displays cytokinin dependent and independent branches. J Integr Plant Biol 58: 226–229
Li P, Zhuang Z, Cai H, Cheng S, Soomro AA, Liu Z, Gu R, Mi G, Yuan L, Chen F (2016b) Use of genotype–environment interactions to elucidate the pattern of maize root plasticity to nitrogen deficiency. J Integr Plant Biol 58: 242–253
Song W, Wang B, Hauck AL, Dong X, Li J, Lai J (2016) Genetic dissection of maize seedling root system architecture traits using an ultrahigh density bin-map and a recombinant inbred line population. J Integr Plant Biol 58: 266–279
Lynch J (1995) Root architecture and plant productivity. Plant Physiol 109: 7–13
Topp CN, Bray AL, Ellis NA, Liu ZB (2016) How can we harness quantitative genetic variation in crop root systems for agricultural improvement? J Integr Plant Biol 58: 213–225
Lynch J (2007) Roots of the second green revolution. Aust J Bot 55: 493–512 Lynch JP (2011) Root phenes for enhanced soil exploration and phosphorus acquisition: Tools for future crops. Plant Physiol 156: 1041–1049
Uga Y, Okuno K, Yano M (2011) Dro1, a major QTL involved in deep rooting of rice under upland field conditions. J Exp Bot 62: 2485–2494
Pachauri KR, Reisinger A (2007) IPCC Fourth Assessment Report: Climate Change 2007-Synthesis Report
Uga Y, Sugimoto K, Ogawa S, Rane J, Ishitani M, Hara N, Kitomi Y, Inukai Y, Ono K, Kanno N, Inoue H, Takehisa H, Motoyama R, Nagamura Y, Wu J, Matsumoto T, Takai T, Okuno K, Yano M (2013) Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions. Nat Genet 45: 1097–1102
Pi~ neros MA, Larson BG, Shaff JE, Schneider DJ, Falc~ ao AX, Yuan L, Clark RT, Craft EJ, Davis TW, Pradier PL, Shaw NM, Assaranurak I, McCouch SR, Sturrock C, Bennett M, Kochian LV (2016)
Wang XR, Shen JB, Liao H (2010) Acquisition or utilization, which is more critical for enhancing phosphorus efficiency in modern crops? Plant Sci 179: 302–306
Lynch JP, Brown KM (2001) Topsoil foraging—an architectural adaptation of plants to low phosphorus availability. Plant Soil 237: 225–237
March 2016 | Volume 58 | Issue 3 | 190–192
www.jipb.net
Journal of Integrative Plant Biology
Free Access
Editorial
Root architecture Numerous research publications over the past 20 years have made it quite clear that a better understanding of the molecular and genetic basis for variation in root system architecture (RSA) will greatly aid the development of crop varieties with improved and more efficient nutrient and water acquisition under limiting conditions. In many parts of the world, especially in developing countries, food security is threatened by drought stress and poor soil fertility, which are major limitations to crop yields. These stresses are increasing in severity as climate change is resulting in more variable and extreme weather events (Pachauri and Reisinger 2007). Furthermore, due to the rising costs for fertilizer production and distribution, and increasing water scarcity, as well as the negative environmental impacts associated with overuse of fertilizers, further increases in crop yields via increased agricultural inputs are not sustainable, nor are they economically viable in many developing countries (Lynch 2007). Thus, identifying how plants control the development of RSA can have a real impact on improving agricultural food production and world food security in the 21st century. There are many ways to describe RSA and probably the simplest definition is that root architecture is the spatial configuration of the entire root system in the soil (Fitter 1987; Lynch 1995). Root architecture can be looked at as the geometric arrangement of the individual roots within a root system in the soil volume the root system occupies. The different classes of root types are often controlled by different gene networks. Via these complex networks of genes and proteins, plants can control root type, and how the different roots are positioned and oriented via regulation of root angle, rate of root growth and degree of root branching. Control of all of these traits helps determine the overall 3D root system architecture. Genetically based variation in different RSA traits within and across plant species has been clearly linked to improved water and mineral nutrient acquisition. Thus, it is important that we better understand how plants control their RSA and use this knowledge to increase crop plant yields and water/nutrient acquisition efficiency (Berntson 1994; Lynch 2011). The world is facing an impending food crisis as we have to increase food production by 70% in the next 30–40 years to feed a world population estimated to be 9.5 billion by the year 2050. Much of this population growth is occurring in developing countries which already deal with food production problems due to agriculture on predominately nutrient-poor and water-limited soils. Therefore, 21st century agriculture will depend on the breeding of crops with improved RSA as well as enhanced root health and function, to enable significantly increased crop yields using less water and fertilizers, in order for agriculture to be carried out in a more sustainable and environmentally friendly manner. With regard to the role of RSA in more efficient nutrient acquisition, much of the pioneering work involved phosphorous (P) acquisition and P efficiency (the genetically based ability of certain genotypes to maintain higher yields on low
March 2016 | Volume 58 | Issue 3 | 190–192
P soils). P is probably the most limiting mineral nutrient and it is also the least mobile mineral nutrient in the soil, as the phosphate anion can bind tightly to iron and aluminum oxides on the surface of clay minerals, and forms insoluble precipitates with calcium, and can be tied up as organic P. High soil P fixation is a particular problem in the tropics and subtropics where the highly weathered acid soils tie up most of the P in the surface horizons of the soil (Kochian et al. 2005). Thus, in order to mine this fixed P from the soil, the plant must modify its RSA to place more lateral roots into the surface soil region and then alter the rhizosphere soil around these roots to solubilize and absorb the soil P. It has long been documented that the root systems of all plant species that have been studied undergo alterations in RSA in response to P deficiency. Through the pioneering work on top soil P foraging in bean and soybean by researchers such as Jonathan Lynch of Penn State University and Hong Liao of Fujian Agriculture and Forestry University, China, it has been shown that one of the major traits of P-efficient genotypes is the generation of ageotropic lateral roots with more shallow root angles, thus positioning more lateral roots in the surface soil horizons in order to mine the P fixed in these surface soil layers (Lynch and Brown 2001; Lynch 2007; Wang et al. 2010). Furthermore, these researchers have shown it is possible to introgress this root trait into root systems, generating bean and soybean varieties that maintain higher yields on low P soils. More recently, a research team led by Sigrid Heuer of the International Rice Research Institute and Matthias Wissuwa of the Japan International Research Center for Agricultural Sciences, cloned the first P uptake efficiency gene, Pstol1 (for phosphorous-starvation tolerance 1). Pstol1 encodes a receptor kinase which functions to help increase proliferation of finer lateral roots in the P-efficient genotypes. Subsequently, via a combination of association genetics-based candidate gene analysis and high throughput digital imaging of sorghum root morphology and architecture, Hufnagel et al. (2014) showed that in sorghum, P efficiency is conditioned by several homologues of rice Pstol1 which function to increase proliferation of longer and finer sorghum lateral roots. The most mobile nutrient in the soil is also the one most needed by plants—water. Recently, Yusaku Uga and his team at National Institute of Agrobiological Science in Tsukuba, Japan, used genetic mapping to identify a major root angle quantitative trait locus (QTL) in rice, (DRO1–for Deeper rooting 1) and then cloned the DRO1 gene responsible for this QTL via fine-scale mapping (Uga et al. 2011, 2013). The DRO1 protein was annotated as an unknown protein. Uga and coworkers characterized its function in deeper rooting varieties, near isogenic lines and transgenic lines and showed it triggered deeper root angles for rice crown roots. They showed that DRO1 expression was negatively regulated by auxin and is involved in auxin redistribution in the root tip, leading to asymmetric cell expansion and downward bending of the root in response to gravity. Most importantly with
www.jipb.net
Editorial regard to crop improvement, they showed that backcross introgression of the superior DRO1 allele into shallow rooting rice varieties led to deeper rooting varieties with substantially improved shoot biomass production and grain yields in response to moderate and severe drought stress. In this JIPB special issue on root architecture, we present three invited expert reviews, one research letter and four research papers. In the review by Li et al. (2016a) entitled “Improving crop nutrient efficiency through root architecture modifications”, the authors summarize and analyze the published literature regarding the role of root system architecture in more efficient acquisition of N and P, the two most limiting mineral nutrients for crop production. The physiological and molecular regulation of changes in root architecture that enhance N and P uptake and accumulation under limiting conditions is reviewed. Then the authors look at the state of our understanding of the interplay of root architecture with the root microbiome, with a focus on the two best understood root-microbial associations, rhizobial-based N2 fixation and root-mycorhizzal symbioses. The most recently discovered plant hormone, strigalactone, is known to play roles in root development. In the review by Kapulnik and Koltai (2016) entitled “Fine-tuning by strigolactones of root response to low phosphate”, the authors show how this hormone plays a role in communication between roots and mycorhizzal fungi, especially under P-limiting conditions. It appears that strigalactones are involved in communications between the root system and root microbiome, to help facilitate the colonization of roots by P-acquiring mycorrhizae. Finally, the review by Topp et al. (2016) entitled “How can we harness quantitative genetic variation in crop root system architecture for agricultural improvement?” addresses the new technologies that are emerging and being employed to image roots and quantify root traits grown in both transparent growth media and soils. Then, the authors review the literature on mining the digital root phenotypic data to genetically map root system architecture, how to use the results to better understand the molecular basis for variation in RSA, and finally, to breed for crops with improved root traits. The five research papers deal with a range of topics, including new technologies to image and quantify root architecture traits, the development of improved genetic resources to genetically map and dissect complex RSA traits, the interplay of nutrient status, hormones, and modification of RSA for N acquisition efficiency. The research paper by Pi~ neros et al. (2016) entitled “Evolving technologies for growing, imaging, and analyzing 3D root system architecture of crop plants”, describes recent advances and improvements in a digital optical imaging platform for RSA that enables the users to grow a range of plant species in hydroponics and soil or soil-like media, and generate 3D reconstructions of RSA for quantification of root traits. The paper entitled “Genetic dissection of maize seedling root system architecture traits using an ultra-high density bin-map and a recombinant inbred line population” by Song et al. (2016) employed QTL mapping of maize RSA traits conducted in a maize recombinant inbred line population generated from two widely used maize hybrids. A number of robust RSA QTL were identified and the findings will set the stage for more detailed genetic dissection of these complex traits in lines widely used for maize breeding. www.jipb.net
191
There are three research papers in this special issue addressing different aspects of RSA and N acquisition. In the Ruffel et al. (2016) Letter to the Editor entitled “Longdistance nitrate signaling displays cytokinin dependent and independent branches”, the authors present findings indicating that certain aspects of Arabidopsis lateral root development are under the control of long-distance systemic N signaling and that cytokinins play a role in this signaling. In the research paper entitled “Use of genotype-environment interactions to elucidate the pattern of maize root plasticity to nitrogen deficiency” by Li et al. (2016b), the authors conducted QTL mapping of maize root plasticity in response to changes in N status and found that the complex genetic control of root plasticity in response to changing N nutrition has a significant GE component, but it is possible to begin separating out the genetic component of this interaction for further mapping and possible map-based breeding of improved maize root traits. In the Araya et al. (2016) paper entitled “Statistical modeling of nitrogen-dependent modulation of root system architecture in Arabidopsis thaliana”, a statistical modeling approach was developed to study the responses of RSA to changing N status. The authors are able to begin to provide the statistical framework for a better understanding of the complex dynamics of RSA in response to a changing soil environment and plant N status, in order to begin to dissect out specific root responses in a systematic manner. From the invited reviews and research papers in this special issue on root architecture, I hope the readers will get some sense of this dynamic and rapidly growing and evolving field of research on root system development and function, and the potential for translating the findings from this research into the breeding of crop species with more vigorous, nutrient-efficient and resilient root systems. Leon V. Kochian, Professor Special Issue Editor Robert W. Holley Center for Agriculture and Health, USDA-ARS, Cornell University, Ithaca, NY 14853, USA doi: 10.1111/jipb.12471 © 2016 Institute of Botany, Chinese Academy of Sciences
REFERENCES Araya T, Kubo T, von Wir en N, Takahashi H (2016) Statistical modeling of nitrogen-dependent modulation of root system architecture in Arabidopsis thaliana. J Integr Plant Biol 58: 254–265 Berntson GM (1994) Modelling root architecture: Are there tradeoffs between efficiency and potential of resource acquisition? New Phytol 127: 483–493 Fitter AH (1987) An architectural approach to the comparative ecology of plant root systems. New Phytol 106: 61–77 Hufnagel B, de Sousa SM, Assis L, Guimaraes CT, Leiser W, Azevedo GC, Negri B, Larson BG, Shaff JE, Pastina MM, Barros BA, Weltzien E, Rattunde HF, Viana JH, Clark RT, Falc~ ao A, Gazaffi R, Garcia AA, Schaffert RE, Kochian LV, Magalhaes JV (2014) Duplicate and conquer: Multiple homologs of PHOSPHORUS-STARVATION TOLERANCE1 enhance phosphorus acquisition and sorghum performance on low-phosphorus soils. Plant Physiol 166: 659–677 Kapulnik Y, Koltai H (2016) Fine-tuning by strigolactones of root response to low phosphate. J Integr Plant Biol 58: 203–212
March 2016 | Volume 58 | Issue 3 | 190–192
192
Editorial
Kochian LV, Pi~ neros MA, Hoekenga OA (2005) The physiology, genetics and molecular biology of plant aluminum resistance and toxicity. Plant Soil 274: 175–195
Evolving technologies for growing, imaging, and analyzing 3D root system architecture of crop plants. J Integr Plant Biol 58: 230–241
Li X, Zeng RS, Liao H (2016a) Improving crop nutrient efficiency through root architecture modifications. J Integr Plant Biol 58: 193–202
Ruffel S, Poitout A, Krouk G, Coruzzi GM, Lacombe B (2016) Longdistance nitrate signaling displays cytokinin dependent and independent branches. J Integr Plant Biol 58: 226–229
Li P, Zhuang Z, Cai H, Cheng S, Soomro AA, Liu Z, Gu R, Mi G, Yuan L, Chen F (2016b) Use of genotype–environment interactions to elucidate the pattern of maize root plasticity to nitrogen deficiency. J Integr Plant Biol 58: 242–253
Song W, Wang B, Hauck AL, Dong X, Li J, Lai J (2016) Genetic dissection of maize seedling root system architecture traits using an ultrahigh density bin-map and a recombinant inbred line population. J Integr Plant Biol 58: 266–279
Lynch J (1995) Root architecture and plant productivity. Plant Physiol 109: 7–13
Topp CN, Bray AL, Ellis NA, Liu ZB (2016) How can we harness quantitative genetic variation in crop root systems for agricultural improvement? J Integr Plant Biol 58: 213–225
Lynch J (2007) Roots of the second green revolution. Aust J Bot 55: 493–512 Lynch JP (2011) Root phenes for enhanced soil exploration and phosphorus acquisition: Tools for future crops. Plant Physiol 156: 1041–1049
Uga Y, Okuno K, Yano M (2011) Dro1, a major QTL involved in deep rooting of rice under upland field conditions. J Exp Bot 62: 2485–2494
Pachauri KR, Reisinger A (2007) IPCC Fourth Assessment Report: Climate Change 2007-Synthesis Report
Uga Y, Sugimoto K, Ogawa S, Rane J, Ishitani M, Hara N, Kitomi Y, Inukai Y, Ono K, Kanno N, Inoue H, Takehisa H, Motoyama R, Nagamura Y, Wu J, Matsumoto T, Takai T, Okuno K, Yano M (2013) Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions. Nat Genet 45: 1097–1102
Pi~ neros MA, Larson BG, Shaff JE, Schneider DJ, Falc~ ao AX, Yuan L, Clark RT, Craft EJ, Davis TW, Pradier PL, Shaw NM, Assaranurak I, McCouch SR, Sturrock C, Bennett M, Kochian LV (2016)
Wang XR, Shen JB, Liao H (2010) Acquisition or utilization, which is more critical for enhancing phosphorus efficiency in modern crops? Plant Sci 179: 302–306
Lynch JP, Brown KM (2001) Topsoil foraging—an architectural adaptation of plants to low phosphorus availability. Plant Soil 237: 225–237
March 2016 | Volume 58 | Issue 3 | 190–192
www.jipb.net
