Efficient root systems for enhancing tolerance of crops to water and phosphorus limitation

Development of future crop varieties with efficient root systems for enhanced water and phosphorus uptake is essential for improving crop adaptation and hence food security. Root system architecture (RSA) traits that overcome low-water and low-phosphorus stresses are critical to maintaining structural and functional properties, and are considered the first-order targets in breeding programmes for rainfed environments. Modification of root system architecture could contribute to improvements of desirable agronomic and physiological traits such as biomass, yield, drought resistance, and tolerance to nutrient deficiencies. Advanced phenotyping, imaging, modelling and molecular biotechnologies offer promise in identifying RSA traits for efficient resource acquisition and adaptation to abiotic stresses. This review highlights the complexity and regulation of RSA in response to water and P stresses.

[1]  Tobias Wojciechowski,et al.  Opportunities and challenges in the subsoil: pathways to deeper rooted crops. , 2015, Journal of experimental botany.

[2]  S. Asseng,et al.  Modelling yield losses of aluminium-resistant and aluminium-sensitive wheat due to subsurface soil acidity: effects of rainfall, liming and nitrogen application , 2003, Plant and Soil.

[3]  Ping Wu,et al.  Role of OsPHR2 on phosphorus homoestasis and root hairs development in rice (Oryza sativa L.) , 2008, Plant signaling & behavior.

[4]  G. Hammer,et al.  QTL for nodal root angle in sorghum (Sorghum bicolor L. Moench) co-locate with QTL for traits associated with drought adaptation , 2011, Theoretical and Applied Genetics.

[5]  S. Wilkinson,et al.  Drought, ozone, ABA and ethylene: new insights from cell to plant to community. , 2010, Plant, cell & environment.

[6]  F. Gérard,et al.  Acquisition of phosphorus and other poorly mobile nutrients by roots. Where do plant nutrition models fail? , 2011, Plant and Soil.

[7]  Z. Fei,et al.  Abnormal Physiological and Molecular Mutant Phenotypes Link Chloroplast Polynucleotide Phosphorylase to the Phosphorus Deprivation Response in Arabidopsis1[C][W][OA] , 2009, Plant Physiology.

[8]  Jonathan P. Lynch,et al.  Utility of root cortical aerenchyma under water limited conditions in tropical maize (Zea mays L.) , 2015 .

[9]  R. Richards,et al.  Traits and selection strategies to improve root systems and water uptake in water-limited wheat crops. , 2012, Journal of experimental botany.

[10]  L. Comas,et al.  Root traits contributing to plant productivity under drought , 2013, Front. Plant Sci..

[11]  Zed Rengel,et al.  Phenotyping for Root Traits , 2015 .

[12]  H. Lambers,et al.  The carboxylate-releasing phosphorus-mobilizing strategy can be proxied by foliar manganese concentration in a large set of chickpea germplasm under low phosphorus supply. , 2018, The New phytologist.

[13]  Z. Rengel,et al.  Root trait diversity, molecular marker diversity, and trait-marker associations in a core collection of Lupinus angustifolius , 2016, Journal of experimental botany.

[14]  L. Dolan,et al.  A basic helix-loop-helix transcription factor controls cell growth and size in root hairs , 2010, Nature Genetics.

[15]  P. Pesaresi,et al.  The protein kinase Pstol1 from traditional rice confers tolerance of phosphorus deficiency , 2012, Nature.

[16]  Jonathan P Lynch,et al.  Steep, cheap and deep: an ideotype to optimize water and N acquisition by maize root systems. , 2013, Annals of botany.

[17]  Fusuo Zhang,et al.  Cluster Root Formation by Lupinus Albus is Modified by Stratified Application of Phosphorus in a Split-Root System , 2007 .

[18]  An Yang,et al.  OsMYB2P-1, an R2R3 MYB Transcription Factor, Is Involved in the Regulation of Phosphate-Starvation Responses and Root Architecture in Rice1[C][W][OA] , 2012, Plant Physiology.

[19]  Stephanie Smith,et al.  Root system architecture: insights from Arabidopsis and cereal crops , 2012, Philosophical Transactions of the Royal Society B: Biological Sciences.

[20]  Shawn M. Kaeppler,et al.  Detection of quantitative trait loci for seminal root traits in maize (Zea mays L.) seedlings grown under differential phosphorus levels , 2006, Theoretical and Applied Genetics.

[21]  R. Varshney,et al.  Fast‐Track Introgression of “QTL‐hotspot” for Root Traits and Other Drought Tolerance Traits in JG 11, an Elite and Leading Variety of Chickpea , 2013 .

[22]  E. Blumwald,et al.  Hormone balance and abiotic stress tolerance in crop plants. , 2011, Current opinion in plant biology.

[23]  J. Lynch,et al.  QTL mapping and phenotypic variation for root architectural traits in maize (Zea mays L.) , 2014, Theoretical and Applied Genetics.

[24]  A. Diggle,et al.  Simulating form and function of root systems: efficiency of nitrate uptake is dependent on root system architecture and the spatial and temporal variability of nitrate supply , 2004 .

[25]  M. Yano,et al.  Dro1, a major QTL involved in deep rooting of rice under upland field conditions. , 2011, Journal of experimental botany.

[26]  Johannes A. Postma,et al.  Modelling root plasticity and response of narrow-leafed lupin to heterogeneous phosphorus supply , 2013, Plant and Soil.

[27]  Fusuo Zhang,et al.  Mapping QTLs for root system architecture of maize (Zea mays L.) in the field at different developmental stages , 2012, Theoretical and Applied Genetics.

[28]  A. Verbyla,et al.  Assessing the importance of subsoil constraints to yield of wheat and its implications for yield improvement , 2013, Crop and Pasture Science.

[29]  Ling Zhu,et al.  Transcriptional regulation of PIN genes by FOUR LIPS and MYB88 during Arabidopsis root gravitropism , 2015, Nature Communications.

[30]  Manuel Ruiz,et al.  TropGeneDB, the multi-tropical crop information system updated and extended , 2012, Nucleic Acids Res..

[31]  B. N. Devaiah,et al.  WRKY75 Transcription Factor Is a Modulator of Phosphate Acquisition and Root Development in Arabidopsis1[C][W][OA] , 2007, Plant Physiology.

[32]  K. Siddique,et al.  Characterising root trait variability in chickpea (Cicer arietinum L.) germplasm , 2016, Journal of experimental botany.

[33]  Hiroaki Kusano,et al.  Phosphatidylinositol phosphate 5-kinase genes respond to phosphate deficiency for root hair elongation in Arabidopsis thaliana. , 2015, The Plant journal : for cell and molecular biology.

[34]  Y. Inukai,et al.  QTL associated with lateral root plasticity in response to soil moisture fluctuation stress in rice , 2015, Plant and Soil.

[35]  Jonathan P Lynch,et al.  Root anatomical phenes associated with water acquisition from drying soil: targets for crop improvement. , 2014, Journal of experimental botany.

[36]  Z. Rengel,et al.  Root architecture alteration of narrow-leafed lupin and wheat in response to soil compaction , 2014 .

[37]  Ulrich Schurr,et al.  Future scenarios for plant phenotyping. , 2013, Annual review of plant biology.

[38]  H. Lambers,et al.  Plant adaptations to severely phosphorus-impoverished soils. , 2015, Current opinion in plant biology.

[39]  J. Malamy,et al.  Intrinsic and environmental response pathways that regulate root system architecture. , 2005, Plant, cell & environment.

[40]  Ben Scheres,et al.  Polar PIN Localization Directs Auxin Flow in Plants , 2006, Science.

[41]  G. Neumann,et al.  Cluster roots--an underground adaptation for survival in extreme environments. , 2002, Trends in plant science.

[42]  J. Friml,et al.  Gravity-induced PIN transcytosis for polarization of auxin fluxes in gravity-sensing root cells , 2010, Proceedings of the National Academy of Sciences.

[43]  J. Lynch,et al.  Root hairs confer a competitive advantage under low phosphorus availability , 2001, Plant and Soil.

[44]  H. G. Nimmo,et al.  BHLH32 modulates several biochemical and morphological processes that respond to Pi starvation in Arabidopsis. , 2007, The Biochemical journal.

[45]  François Tardieu,et al.  Any trait or trait-related allele can confer drought tolerance: just design the right drought scenario. , 2012, Journal of experimental botany.

[46]  Jianming Yu,et al.  The genetic architecture of nodal root number in maize , 2018, The Plant journal : for cell and molecular biology.

[47]  K. Noguchi,et al.  Comparison of the response to phosphorus deficiency in two lupin species, Lupinus albus and L. angustifolius, with contrasting root morphology. , 2015, Plant, cell & environment.

[48]  A. Diggle,et al.  Development of a novel semi-hydroponic phenotyping system for studying root architecture. , 2011, Functional plant biology : FPB.

[49]  K. Miura,et al.  The Arabidopsis SUMO E3 ligase SIZ1 controls phosphate deficiency responses. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[50]  H. Liao,et al.  SPX1 is an important component in the phosphorus signalling network of common bean regulating root growth and phosphorus homeostasis , 2014, Journal of experimental botany.

[51]  Dynamical and Microrheological Analysis of Amyloplasts in the Plant Root Gravity-Sensing Cells , 2015 .

[52]  Emma Mace,et al.  QTL for root angle and number in a population developed from bread wheats (Triticum aestivum) with contrasting adaptation to water-limited environments , 2013, Theoretical and Applied Genetics.

[53]  J. H. Manwaring,et al.  Rapid physiological adjustment of roots to localized soil enrichment , 1990, Nature.

[54]  J. Lynch,et al.  New roots for agriculture: exploiting the root phenome , 2012, Philosophical Transactions of the Royal Society B: Biological Sciences.

[55]  J. Lynch,et al.  Topsoil foraging – an architectural adaptation of plants to low phosphorus availability , 2001, Plant and Soil.

[56]  Graeme L. Hammer,et al.  Genotypic variation in seedling root architectural traits and implications for drought adaptation in wheat (Triticum aestivum L.) , 2008, Plant and Soil.

[57]  H. Lambers,et al.  Phosphorus Nutrition of Proteaceae in Severely Phosphorus-Impoverished Soils: Are There Lessons To Be Learned for Future Crops?1 , 2011, Plant Physiology.

[58]  G. Mi,et al.  Comparative Analysis of Root Traits and the Associated QTLs for Maize Seedlings Grown in Paper Roll, Hydroponics and Vermiculite Culture System , 2017, Front. Plant Sci..

[59]  Wendy J. Lyzenga,et al.  Abiotic stress tolerance mediated by protein ubiquitination. , 2012, Journal of experimental botany.

[60]  Jonathan P. Lynch,et al.  Roots of the Second Green Revolution , 2007 .

[61]  J. Lynch.  Root Architecture and Plant Productivity , 1995, Plant physiology.

[62]  S. Salvi,et al.  Two major quantitative trait loci controlling the number of seminal roots in maize co-map with the root developmental genes rtcs and rum1 , 2016, Journal of experimental botany.

[63]  P. Vlek,et al.  Root Architecture and Resource Acquisition: Wheat as a Model Plant , 2013 .

[64]  Yan Liang,et al.  Neglecting legumes has compromised human health and sustainable food production , 2016, Nature Plants.

[65]  Tobias Wojciechowski,et al.  Root phenomics of crops: opportunities and challenges. , 2009, Functional plant biology : FPB.

[66]  A. Karthikeyan,et al.  Ethylene signalling is involved in regulation of phosphate starvation-induced gene expression and production of acid phosphatases and anthocyanin in Arabidopsis. , 2011, The New phytologist.

[67]  J. Lynch,et al.  Root cortical burden influences drought tolerance in maize. , 2013, Annals of botany.

[68]  M. Yano,et al.  Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions , 2013, Nature Genetics.

[69]  H. G. Nimmo,et al.  Identification of an F-box protein that negatively regulates P(i) starvation responses. , 2008, Plant & cell physiology.

[70]  A. Diggle,et al.  Phosphorus starvation boosts carboxylate secretion in P-deficient genotypes of Lupinus angustifolius with contrasting root structure , 2013, Crop and Pasture Science.

[71]  Laurent Nussaume,et al.  Root tip contact with low-phosphate media reprograms plant root architecture , 2007, Nature Genetics.

[72]  Q. Gao,et al.  Overexpression of transcription factor ZmPTF1 improves low phosphate tolerance of maize by regulating carbon metabolism and root growth , 2011, Planta.

[73]  J. Lynch,et al.  Root anatomical phenes predict root penetration ability and biomechanical properties in maize (Zea Mays) , 2015, Journal of experimental botany.

[74]  S. Shabala,et al.  On a quest for stress tolerance genes: membrane transporters in sensing and adapting to hostile soils. , 2016, Journal of experimental botany.

[75]  J. Lynch,et al.  Adaptation of beans (Phaseolus vulgaris L.) to low phosphorus availability , 1995 .

[76]  J. Zhao,et al.  A soybean β-expansin gene GmEXPB2 intrinsically involved in root system architecture responses to abiotic stresses. , 2011, The Plant journal : for cell and molecular biology.

[77]  Jianbo Shen,et al.  Localized application of phosphorus and ammonium improves growth of maize seedlings by stimulating root proliferation and rhizosphere acidification , 2010 .

[78]  J. Bailey-Serres,et al.  Genetic mechanisms of abiotic stress tolerance that translate to crop yield stability , 2015, Nature Reviews Genetics.

[79]  J. Lynch,et al.  Reduced Lateral Root Branching Density Improves Drought Tolerance in Maize1[OPEN] , 2015, Plant Physiology.

[80]  Michelle Watt,et al.  Quantifying the response of wheat (Triticum aestivum L) root system architecture to phosphorus in an Oxisol , 2014, Plant and Soil.

[81]  Fusuo Zhang,et al.  Localized application of NH4+-N plus P at the seedling and later growth stages enhances nutrient uptake and maize yield by inducing lateral root proliferation , 2013, Plant and Soil.

[82]  P. Langridge,et al.  Breeding Technologies to Increase Crop Production in a Changing World , 2010, Science.

[83]  X. Draye,et al.  Root system architecture: opportunities and constraints for genetic improvement of crops. , 2007, Trends in plant science.

[84]  J. Chory,et al.  Unraveling the paradoxes of plant hormone signaling integration , 2010, Nature Structural &Molecular Biology.

[85]  H. Liao,et al.  Improving crop nutrient efficiency through root architecture modifications. , 2016, Journal of integrative plant biology.

[86]  Xiaolong Yan,et al.  Genetic mapping of basal root gravitropism and phosphorus acquisition efficiency in common bean. , 2004, Functional plant biology : FPB.

[87]  C. Vance,et al.  Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. , 2003, The New phytologist.

[88]  M. Estelle,et al.  Recent advances and emerging trends in plant hormone signalling , 2009, Nature.

[89]  H. Bohnert,et al.  SIZ1 Regulation of Phosphate Starvation-Induced Root Architecture Remodeling Involves the Control of Auxin Accumulation1[C][W][OA] , 2010, Plant Physiology.

[90]  J. York,et al.  Generation of phytate-free seeds in Arabidopsis through disruption of inositol polyphosphate kinases. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[91]  Philip N Benfey,et al.  From lab to field, new approaches to phenotyping root system architecture. , 2011, Current opinion in plant biology.

[92]  Malachy T. Campbell,et al.  Introgression of Novel Traits from a Wild Wheat Relative Improves Drought Adaptation in Wheat1[W] , 2013, Plant Physiology.

[93]  F. Zhao,et al.  ABA plays essential roles in regulating root growth by interacting with auxin and MAPK signaling pathways and cell-cycle machinery in rice seedlings , 2015, Plant Growth Regulation.

[94]  Fusuo Zhang,et al.  Root morphological responses to localized nutrient supply differ among crop species with contrasting root traits , 2013, Plant and Soil.

[95]  J. J. Camacho-Cristóbal,et al.  PRD, an ArabidopsisAINTEGUMENTA-like gene, is involved in root architectural changes in response to phosphate starvation , 2008, Planta.

[96]  J. Léon,et al.  Wild barley introgression lines revealed novel QTL alleles for root and related shoot traits in the cultivated barley (Hordeum vulgareL.) , 2014, BMC Genetics.