Root morphology and rhizosheath acid phosphatase activity in legume and graminoid species respond differently to low phosphorus supply

Akhtar, 2016, Phosphorus stress-induced differential growth, and phosphorus acquisition and use efficiency by spring wheat cultivars, Commun. Soil Sci. Plant Anal., 47, 15, 10.1080/00103624.2016.1232089 Anuradha, 1991, Promotion of root elongation by phosphorus deficiency, Plant Soil, 136, 273, 10.1007/BF02150060 Ao, 2010, Genetic variability for root morph-architecture traits and root growth dynamics as related to phosphorus efficiency in soybean, Funct. Plant Biol., 37, 304, 10.1071/FP09215 Carvalhais, 2011, Root exudation of sugars, amino acids, and organic acids by maize as affected by nitrogen, phosphorus, potassium, and iron deficiency, J. Plant Nutr. Soil Sci., 174, 3, 10.1002/jpln.201000085 Chen, 2017, Characterising root trait variability in chickpea (Cicer arietinum L.) germplasm, J. Exp. Bot., 68, 1987 Chen, 2020, Phenotypic variability in bread wheat root systems at the early vegetative stage, BMC Plant Biol., 20, 185, 10.1186/s12870-020-02390-8 Chen, 2018, Efficient root systems to enhance crop tolerance to water and phosphorus limitation, Indian J. Plant Physiol., 23, 689, 10.1007/s40502-018-0415-3 Chen, 2016, Root trait diversity, molecular marker diversity and trait-marker associations in a core collection of Lupinus angustifolius, J. Exp. Bot., 67, 3683, 10.1093/jxb/erw127 Chen, 2013, Modelling root plasticity and response of narrow-leafed lupin to heterogeneous phosphorus supply, Plant Soil, 372, 319, 10.1007/s11104-013-1741-x Chen, 2011, Development of a novel semi-hydroponic phenotyping system for studying root architecture, Funct. Plant Biol., 38, 355, 10.1071/FP10241 Chen, 2012, Assessing variability in root traits of wild Lupinus angustifolius germplasm: basis for modelling root system structure, Plant Soil, 354, 141, 10.1007/s11104-011-1050-1 Chen, 2013, Phosphorus starvation boosts carboxylate secretion in P-deficient genotypes of Lupinus angustifolius with contrasting root structure, Crop Pasture Sci., 64, 588, 10.1071/CP13012 Denton, 2006, Root distributions of Australian herbaceous perennial legumes in response to phosphorus placement, Funct. Plant Biol., 33, 1091, 10.1071/FP06176 Fan, 2015, Changes in root morphology and physiology to limited phosphorus and moisture in a locally-selected cultivar and an introduced cultivar of Medicago sativa L. growing in alkaline soil, Plant Soil, 392, 215, 10.1007/s11104-015-2454-0 Figueroa-Bustos, 2019, Early season drought largely reduces grain yield in wheat cultivars with smaller root systems, Plants, 8, 305, 10.3390/plants8090305 Florez-Sarasa1, 2014, The alternative respiratory pathway mediates carboxylate synthesis in white lupin cluster roots under phosphorus deprivation, Plant Cell Environ., 37, 922, 10.1111/pce.12208 Hammond, 2008, Sucrose transport in the phloem: integrating root responses to phosphorus starvation, J. Exp. Bot., 59, 93, 10.1093/jxb/erm221 Hermans, 2006, How do plants respond to nutrient shortage by biomass allocation?, Trends Plant Sci., 11, 610, 10.1016/j.tplants.2006.10.007 Hinsinger, 2001, Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review, Plant Soil, 237, 173, 10.1023/A:1013351617532 Holford, 1997, Soil phosphorus: its measurement, and its uptake by plants, Aust. J. Soil Res., 35, 227, 10.1071/S96047 Johnston, 2014, Phosphorus: its efficient use in agriculture, Adv. Agron., 123, 177, 10.1016/B978-0-12-420225-2.00005-4 Kouas, 2009, Root Proliferation, proton efflux, and acid phosphatase activity in common bean (Phaseolus vulgaris) under phosphorus shortage, J. Plant Biol., 52, 395, 10.1007/s12374-009-9050-x Lambers, 2015, Plant adaptations to severely phosphorus-impoverished soils, Curr. Opin. Plant Biol., 25, 23, 10.1016/j.pbi.2015.04.002 Lambers, 2006, Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits, Ann. Bot., 98, 693, 10.1093/aob/mcl114 Liao, 2000, Adaptive changes and genotypic variation for root architecture of common bean in response to phosphorus deficiency, Acta Bot. Sin., 42, 158 Liu, 2000, Acquisition of Cu, Zn, Mn and Fe by mycorrhizal maize (Zea mays L.) grown in soil at different P and micronutrient levels, Mycorrhiza, 9, 331, 10.1007/s005720050277 Liu, 2016, The effects of nitrogen form on root morphological and physiological adaptations of maize, white lupin and faba bean under phosphorus deficiency, AoB Plants, 8, plw058, 10.1093/aobpla/plw058 Lynch, 2011, Root phenes for enhanced soil exploration and phosphorus acquisition: tools for future crops, Plant Physiol., 156, 1041, 10.1104/pp.111.175414 Lynch, 2019, Root phenotypes for improved nutrient capture: an underexploited opportunity for global agriculture, New Phytol., 223, 548, 10.1111/nph.15738 Lyu, 2016, Major crop species show differential balance between root morphological and physiological responses to variable phosphorus supply, Front. Plant Sci., 7, 1939, 10.3389/fpls.2016.01939 Manske, 2000, Traits associated with improved P-uptake efficiency in CIMMYT's semidwarf spring bread wheat grown on an acid Andisol in Mexico, Plant Soil, 221, 189, 10.1023/A:1004727201568 Mayzlish-Gati, 2012, Strigolactones are involved in root response to low phosphate conditions in Arabidopsis, Plant Physiol., 160, 1329, 10.1104/pp.112.202358 Moll, 1982, Analysis and interpretation of factors which contribute to efficiency of nitrogen utilization, Agron. J., 74, 562, 10.2134/agronj1982.00021962007400030037x Murphy, 1962, A modified single solution method for the determination of phosphate in natural waters, Anal. Chim. Acta, 27, 31, 10.1016/S0003-2670(00)88444-5 Neumann, 2000, Physiological aspects of cluster root function and development in phosphorus-deficient white lupin (Lupinus albus L.), Ann. Bot., 85, 909, 10.1006/anbo.2000.1135 Neumann, 1999, Physiological adaptations to phosphorus deficiency during proteoid root development in white lupin, Planta, 208, 373, 10.1007/s004250050572 Nguyen, 2019, Variation in root system architecture and morphology of two wheat genotypes is a predictor of their tolerance to phosphorus deficiency, Acta Physiol. Plant., 41, 109, 10.1007/s11738-019-2891-0 Nielsen, 2001, The effect of phosphorus availability on the carbon economy of contrastingcommon bean (Phaseolus vulgaris L.) genotypes, J. Exp. Bot., 52, 329 Niu, 2013, Responses of root architecture development to low phosphorus availability: a review, Ann. Bot., 112, 391, 10.1093/aob/mcs285 Nuruzzaman, 2005, Phosphorus benefits of different legume crops to subsequent wheat grown in different soils of Western Australia, Plant Soil, 271, 175, 10.1007/s11104-004-2386-6 Ostonen, 2007, Specific root length as an indicator of environmental change, Plant Biosyst., 141, 426, 10.1080/11263500701626069 Palta, 1993, Postanthesis remobilisation and losses of nitrogen in wheat in relation to applied nitrogen, Plant Soil, 155, 179, 10.1007/BF00025013 Palta, 2018, Crop root system traits cannot be seen as a silver bullet delivering drought resistance, Plant Soil, 439, 31, 10.1007/s11104-018-3864-6 Pearse, 2006, Triticum aestivum shows a greater biomass response to a supply of aluminium phosphate than Lupinus albus, despite releasing fewer carboxylates into the rhizosphere, New Phytol., 169, 515, 10.1111/j.1469-8137.2005.01614.x Pooniya, 2020, Impact of the TaMATE1B gene on above and below-ground growth of durum wheat grown on an acid and Al 3+-toxic soil, Plant Soil, 447, 73, 10.1007/s11104-019-04231-6 Qiao, 2019, Dissecting root trait variability in maize genotypes using the semi-hydroponic phenotyping platform, Plant Soil, 439, 75, 10.1007/s11104-018-3803-6 Raghothama, 2005, Phosphate acquisition, Plant Soil, 274, 37, 10.1007/s11104-004-2005-6 Ramaekers, 2010, Strategies for improving phosphorus acquisition efficiency of crop plants, Field Crop. Res., 117, 169, 10.1016/j.fcr.2010.03.001 Ren, 2019, Arbuscular mycorrhizal fungus alters root-sourced signal (abscisic acid) for better drought acclimation in Zea mays L. seedlings, Environ. Exp. Bot., 167, 103824, 10.1016/j.envexpbot.2019.103824 Rengel, 2002, Genetic control of root exudation, Plant Soil, 245, 59, 10.1023/A:1020646011229 Richardson, 2009, Plant mechanisms to optimise access to soil phosphorus, Crop Pasture Sci., 60, 124, 10.1071/CP07125 Rose, 2011, The frustration with utilization: why have improvements in internal phosphorus utilizationefficiency in crops remained so elusive?, Front. Plant Sci., 2, 73, 10.3389/fpls.2011.00073 Santoro, 2020, Strigolactones control root system architecture and tip anatomy in Solanum lycopersicum L. plants under P starvation, Plants, 9, 612, 10.3390/plants9050612 Schenk, 2002, Rooting depths, lateral root spreads and below-ground/above-ground allometries of plants in water-limited ecosystems, J. Ecol., 90, 480, 10.1046/j.1365-2745.2002.00682.x Shen, 2011, Phosphorus dynamics: from soil to plant, Plant Physiol., 156, 997, 10.1104/pp.111.175232 Shen, 2013, Maximizing root/rhizosphere efficiency to improve crop productivity and nutrient use efficiency in intensive agriculture of China, J. Exp. Bot., 64, 1181, 10.1093/jxb/ers342 Shi, 2017, Mycorrhizal relationship in lupines: a review, Legume Res., 40, 965 Silva, 2016, Phosphorus uptake efficiency, root morphology and architecture in Brazilian wheat cultivars, J. Radioanal. Nucl. Chem., 307, 1055, 10.1007/s10967-015-4282-3 Simpson, 2011, Strategies and agronomic interventions to improve the phosphorus-use efficiency of farming systems, Plant Soil, 349, 89, 10.1007/s11104-011-0880-1 Suriyagoda, 2012, Growth, carboxylate exudates and nutrient dynamics in three herbaceous perennial plant species under low, moderate and high phosphorus supply, Plant Soil, 358, 100, 10.1007/s11104-012-1311-7 Suriyagoda, 2010, Multiple adaptive responses of Australian native perennial legumes with pasture potential to grow in phosphorus- and moisture-limited environments, Ann. Bot., 105, 755, 10.1093/aob/mcq040 Ushio, 2015, Linkage of root physiology and morphology as an adaptation to soil phosphorus impoverishment in tropical montane forests, Funct. Ecol., 29, 1235, 10.1111/1365-2435.12424 Vance, 2003, Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource, New Phytol., 157, 423, 10.1046/j.1469-8137.2003.00695.x Vitousek, 2010, Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen-phosphorus interactions, Ecol. Appl., 20, 5, 10.1890/08-0127.1 Wang, 2020, Arbuscular mycorrhizas regulate photosynthetic capacity and antioxidant defense systems to mediate salt tolerance in maize, Plants, 9, 1430, 10.3390/plants9111430 Wang, 2020, Heterogeneous phosphate supply influences maize lateral root proliferation by regulating auxin redistribution, Ann. Bot., 125, 119, 10.1093/aob/mcz154 Wang, 2010, Acquisition or utilization, which is more critical for enhancing phosphorus efficiency in modern crops?, Plant Sci., 179, 302, 10.1016/j.plantsci.2010.06.007 Watt, 2003, Phosphorus acquisition from soil by white lupin (Lupinus albus L.) and soybean (Glycine max L.), species with contrasting root development, Plant Soil, 248, 271, 10.1023/A:1022332700686 Wen, 2019, Tradeoffs among root morphology, exudation and mycorrhizal symbioses for phosphorus-acquisition strategies of 16 crop species, New Phytol., 223, 882, 10.1111/nph.15833 Wen, 2017, Maize responds to low shoot P concentration by altering root morphology rather than increasing root exudation, Plant Soil, 416, 377, 10.1007/s11104-017-3214-0 Yadav, 2001, Influence of organic and inorganic phosphorus supply on the maximum secretion of acid phosphatase by plants, Biol. Fertil. Soils, 34, 140, 10.1007/s003740100376 Zhu, 2017, Inoculation of arbuscular mycorrhizal fungi with plastic mulching in rainfed wheat: a promising farming strategy, Field Crop. Res., 204, 229, 10.1016/j.fcr.2016.11.005 Zhu, 2001, Phosphorus (P) efficiencies and mycorrhizal responsiveness of old and modern wheat cultivars, Plant Soil, 237, 249, 10.1023/A:1013343811110