The importance of the root system of agricultural crops in the conditions of climate change and resource scarcity

Keywords: root system architecture, productivity, stress, influence of external factors, genotypes

Abstract

Introduction. Climate change has led to frequent extreme weather events, especially irregular rainfall. This causes biotic and abiotic stresses in agricultural plants, which negatively affect their productivity. The results. The analysis of the literature showed that the structure of the root system (RSA) is a powerful indicator that reflects the supply of nutrients to plants, as well as for determining its corresponding responses to external factors. It plays a vital role in the productivity and adaptation of plants to different environments and has a central role in the productivity and stability of all plant ecosystems in their ability to exist, in general. Therefore, there is growing recognition that future yield gains can be achieved by optimizing RSA. The main elements of the RSA architecture are the length of the primary root, the density of the lateral roots and at what angle they are located in the soil in relation to the tap root, and the diameter of the roots. External factors, such as the availability of water and nutrients, regulate the formation of lateral and secondary roots, and depending on this, they can spread shallowly or go deep. Genotypes with greater branching, lateral root density and taproot length and high yield are considered deep rooted and suitable for water and nitrogen stressed environments, while genotypes with less lateral branching density and shallowness are suitable for low phosphorus environments. The architecture of the root system is influenced by microorganisms: bacteria and fungi that cause many modifications in the morphology of the roots, depending on the culture, the strain of rhizobacteria PGPR and the type of mycorrhizal fungi AMF. A common feature of Rhizobacteria PGPR is the modification of lateral roots. Conclusion. The use of mycorrhizal fungi AMF increases the degree of root branching, increasing the total length, surface area and volume of roots. Direct phenotyping remains an urgent problem. To solve this problem, the following methods are distinguished: well-controlled laboratory methods that allow automatic phenotyping of RSA, moderately controlled greenhouse and field methods where mature root systems are studied in real soil conditions in the field using an integrated method: visual assessment, manual measurements and image analysis with using 2D, 3D.

References

1. Atkinson J.A., Rasmussen A., Traini R., Voß U., Sturrock C. and et al. Branching Out in Roots: Uncovering Form, Function, and Regulation. Plant Physiol., 2014, Vol. 166. Р.538-550. https://doi.org/10.1104/pp.114.245423.
2. Atkinson J.A., Pound M.P., Bennett M.J., Wells D.M. Uncovering the hidden half of plants using new advances in root phenotyping. Curr. Opin. Biotechnol., 2019, Vol. 55. P. 1–8. https://doi.org/10.1016/j.copbio.2018.06.002.
3. Bao Y., Aggarwal P., Robbins N.E., Sturrock C.J., Thompson M.C. and et al. Plant roots use a patterning mechanism to position lateral root branches toward available water. Proc. Natl. Acad. Sci. U.S.A., 2014, Vol. 111. P. 9319–9324. https://doi.org/10.1073/pnas.1400966111.
4. Barea J.M., Tobar R.M., Azcon-Aguilar C. Effect of a Genetically Modified Rhizobium meliloti Inoculant on the Development of Arbuscular Mycorrhizas, Root Morphology, Nutrient Uptake and Biomass Accumulation in Medicago sativa. New Phytol., 1996, Vol. 134. P. 361-369. https://doi.org/10.1111/j.1469-8137.1996. tb04641.x.
5. Bellini C., Pacurar D.I., Perrone I. Adventitious roots and lateral roots: similarities and differences. Annu Rev Plant Biol., 2014, Vol. 65. P. 639–666. https://doi. org/10.1146/annurev-arplant-050213-035645.
6. Benjamin D.G., Ricardo F.H.G., Swetlana F., von Nicolaus W. Plasticity of the Arabidopsis root system under nutrient deficiencies. Plant Physiology, 2013, Vol. 163. P. 161–179. https://doi.org/10.1104/pp.113.218453.
7. Berta G., Fusconi A., Trotta A., Scannerini S. Morphogenetic modifications induced by the mycorrhizal fungus Glomus isolate E3 in the root system of Allium porrum L. New Phytol., 1990, Vol. 114. P. 207-215. https://dx.doi.org/10.1111/j.1469-8137.1990.tb00392.x.
8. Brundrett M.C., Ferguson B.J., Gressshoff P.M., Mathesius U., Munns A. et al. Chapter 4: Nutrient uptake from soils Chapter editors: Rana Munns and Susanne Schmidt Contributing. РР. 1-59. Australian Society of Plant Scientists, New Zealand Society of Plant Biologists, and New Zealand Institute of Agricultural and Horticultural Science 2010–2018.
9. Bucksch A., Burridge J., York L.M., Das A., Nord E. and et al. Image-based high-throughput field phenotyping of crop roots. Plant Physiology., 2014, Vol. 166, Issue 2. P. 470–486. https://doi.org/10.1104/pp.114.243519.
10. Bui K.T., Naruse T., Yoshida H., Toda Y., Omori Y. and et al. Effects of irrigation on root growth and development of soybean: A 3-year sandy field experiment. Front. Plant Sci., 2022, Vol. 13. 1047563. https://doi.org/10.3389/fpls.2022.1047563
11. Burridge J., Jochua C.N., Bucksch A., Lynch J.P. Legume shovelomics: high-throughput phenotyping of common bean (Phaseolus vulgaris L.) and cowpea (Vigna unguiculata subsp, unguiculata) root architecture in the field. Field Crops Research., 2016, Vol. 192. P. 21–32. https://doi.org/10.1016/j.fcr.2016.04.008.
12. Camilo S., Odindo A.O., Kondwakwenda A. and Sibiya J. Root Traits Related with Drought and Phosphorus Tolerance in Common Bean (Phaseolus vulgaris L.). Agronomy, 2021, Vol. 11. P. 552. https://doi.org/10.3390/agronomy11030552.
13. Casimiro I.T., Beeckman N., Graham R., Bhalerao H., Zhang P. and et al. Dissecting Arabidopsis lateral root development. Trends Plant Sci., 2003, Vol. 8. P. 165-17. https://doi.org/10.1016/S1360-1385(03)00051-7
14. Christopher J., Christopher M., Jennings R., Jones S., Fletcher S. and et al. QTL for root angle and number in a population developed from bread wheat (Triticum aestivum) with contrasting adaptation to waterlimited environments. Theor. Appl. Genet., 2013, Vol. 126. P. 1563–1574. https://doi.org/10.1007/s00122-013-2074-0.
15. Cruz C., Green J.J., Watson C.A., Wilson F., Martins-Loução M.A. Functional aspects of root architecture and mycorrhizal inoculation with respect to nutrient uptake capacity. Mycorrhiza, 2004, Vol. 14. P. 177-184. https://dx.doi.org/10.1007/s00572-003-0254-5
16. Dathe A., Postma J., Postma-Blaauw M. and Lynch, J. Impact of axial root growth angles on nitrogen acquisition in maize depends on environmental conditions. Ann. Bot., 2016, Vol. 118. P. 401–414. https://doi.org/10.1093/aob/mcw112.
17. Del Bianco M., Kepinski S. Building a future with root architecture. Journal of Experimental Botany, 2018, Vol. 69, No. 22. P. 5319–5323. https://doi.org/10.1093/jxb/ery390.
18. Den Herder G., Van Isterdael G., Beeckman T., De Smet I. The roots of a new green revolution. Trends Plant Sci., 2010, Vol. 15. P. 600–607. https://doi.org/10.1016/j.tplants.2010.08.009.
19. Desbrosses G., Bouffaud M.L., Touraine B., Moënne-Loccoz Y., Muller D. and et al. Plant growth-promoting rhizobacteria and root system functioning. Front. PlantSci., 2013, Vol. 4. P. 356. https://doi.org/10.3389/fpls.2013.00356.
20. Ding Z., Fu L., Tie W., Yan Y., Wu C. and et al. Highly dynamic, coordinated, and stage-specific profiles are revealed by a multi-omics integrative analysis during tuberous root development in cassava. J. Expt. Bot., 2020, Vol. 71. P. 7003–7017. https://doi.org/10.1093/jxb/eraa369
21. Dobbelaere S., Croonenborghs A., Thys A., Broek, A.V. and Vanderleyden J. Phytostimulatory effect of A. brasilense wild type and mutant strains altered in IAA production on wheat. Plant Soil., 1999, Vol. 212, P. 155–164. https://doi.org/10.1023/a:1004658000815.
22. Dunbabin V., Diggle A. and Rengel Z. Is there any optimal root architecture for nitrate capture in leaching environments? Plant Cell Environ., 2003, Vol. 26. P. 835–844. https://doi.org/10.1046/j.1365-3040.2003.01015.x.
23. Egamberdieva D., Wirtha S., Jabborovac D., Räsänend L.A. and Liaoe H. Coordination between Bradyrhizobium and Pseudomonas alleviates salt stress in soybean through altering root system architecture. Journal of plant interactions., 2017, Vol. 12, No. 1. P. 100–107 https://doi.org/10.1080/17429145.2017.1294212/
24. El-Khawas H. and Adachi K. Identification and quantification of auxins in culture media of Azospirillum and Klebsiella and their effect on rice roots. Biol. Fertil. Soils, 1999, Vol. 28. P. 377–381. https://doi.org/10.1007/s003740050507.
25. Falk K.G., Jubery T.Z., O’Rourke J.A., Singh A., Sarkar S. and et al. Soybean root system architecture trait study through genotypic, phenotypic, and shapebased clusters. Plant Phenom., 2020, Vol. 2020. 1925495. https://doi.org/10.34133/2020/192549.
26. FAO. (2021) http://www.FAO.org/hunger/en
27. Fenta B.A., Beebe S.E., Kunert K.J., Burridge J.D., Barlow K.M. and et al. Field Phenotyping of Soybean Roots for Drought Stress Tolerance. Agronomy, 2014, Vol. 4, Issue 3. P. 418-435. https://doi.org/10.3390/agronomy4030418.
28. Fukaki H, Tasaka M. Hormone interactions during lateral root formation. Plant Molecular Biology, 2009, Vol. 69, Issue 4. P. 437–449. https://doi.org/10.1007/s11103-008-9417-2.
29. Garciaa J., Schmidta J.E., Gidekelc M. and Gaudin A.C.M. Impact of an antarctic rhizobacterium on root traits and productivity of soybean (Glycine max L.). Journal of plant nutrition, 2021, Vol. 44, No. 12. P. 1818–1825. ttps://doi.org/10.1080/01904167.2021.1884704.
30. Gonin M., Salas-González I., Gopaulchan D. and Castrillo G. Plant microbiota controls an alternative root branching regulatory mechanism in plants. Proc. Natl. Acad. Sci. U.S.A., 2023, Vol. 120. P. 1–10. https://doi.org/10.1073/pnas.2301054120.
31. Gregory P.J., Hutchison D.J., Read D.B. and et al. Non-invasive imaging of roots with highresolution X-ray micro-tomography. Plant Soil, 2023, Vol. 255. P. 351–359. https://doi.org/10.1023/A:1026179919689.
32. Gutjahr C., Casieri L. and Paszkowskі U. Glomus intraradices induces changes in root system architecture of rice independently of common symbiosis signaling. New Phytologist, 2009, Vol. 182. P. 829–837. https://doi.org/10.1111/j.1469-8137.2009.02839.x.
33. Hannah M. Schneider and Lynch J.P. Should Root Plasticity Be a Crop Breeding Target? Front. Plant Sci., 2020, Vol. 11. P. 546. https://doi.org/10.3389/fpls.2020.00546.
34. Ho M.D., Rosas J.C., Brown K.M. and Lynch J.P. Root architectural tradeoffs for water and phosphorus acquisition. Functional Plant Biology, 2005, Vol. 32, Issue 8. P. 737-748 https://doi.org/10.1071/FP05043.
35. Hochholdinger F., Park W.J., Sauer M., Woll K. From weeds to crops: genetic analysis ofroot development in cereals. Trends Plant Sci., 2004, Vol. 9. P. 42–48. https://doi.org/10.1016/j.tplants.2003.11.003
36. Iyer-Pascuzzi A.S., Symonova O., Mileyko Y. and et al. Imaging and analysis platform for automatic phenotyping and trait ranking of plant root systems. Plant physiology, 2010, Vol. 152, Issue 3. P. 1148–1157. https://doi.org/10.1104/pp.109.150748.
37. Jaizme-Vega M.C., Rodríguez-Romero A.S. and Piñero Guerra M.S. Effect of arbuscular mycorrhizal fungi (amf) and other rhizosphere microorganisms on development of the banana root system. Journal of Applied. Pharmaceutical Science, 2016, Vol. 6, Issue 06. P. 131-138. https://doi.org/10.7324/JAPS.2016.60623.
38. Janiak A., Kwaśniewski M., Szarejko I. Gene expression regulation in roots under drought. Journal of Experimental Botany, 2016, Vol. 67. P. 1003–1014. https://doi.org/10.1093/jxb/erv512
39. Jensen E.S., Chongtham I.R., Dhamala N.R., Rodriguez C., Carton N. and Carlsson G. J. Diversifying European agricultural systems by intercropping grain legumes and cereals. Agric. Nat. Resour., 2020, Vol. 47, Issue 3. P. 174-186. https://doi.org/10.7764/ijanr.v47i3.2241
40. Jensen E.S., Peoples M.B., Hauggaard-Nielsen H. Faba bean in cropping systems. Field Crops Res., 2010, Vol. 115, Issue 3. P. 203-216. https://doi.org/10.1016/j.fcr.2009.10.008.
41. Karlova R., Boer D., Hayes S. and Testerink C. Root plasticity under abiotic stress. Plant Physiol., 2021, Vol. 187, Issue 3. P. 1057–1070. https://doi.org/10.1093/plphys/kiab39.
42. Khan M.A., Dorcus C. Gemenet and Arthur Villordon Root System Architecture and Abiotic Stress Tolerance: Current Knowledge in Root and Tuber Crops. Plant Sci., 2016, Vol. 7. P. 2016. https://doi.org/10.3389/fpls.2016.01584
43. Kim S.H., Subramanian P., Hahn B.S. and Ha B.K. High-Throughput Phenotypic Characterization and Diversity Analysis of Soybean Roots (Glycine max L.). Plants, 2022, Vol. 11, Issue 15. P. 2017. https://doi.org/10.3390/plants11152017.
44. Koevoets I.T., Venema J.H., Elzenga J.T.M. and Testerink C. Roots withstanding their environment: exploiting root system architecture responses toabiotic stress to improve crop tolerance. Front. Plant Sci., 2016, Vol. 7. https://doi.org/10.3389/fpls.2016.01335.
45. Krouk G., Lacombe B., Bielach A., Perrine-Walker F., Malinska K. and et al. Nitrate- regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Development Cell, 2010, Vol. 18. P. 927–937. https://doi.org/10.1016/j.devcel.2010.05.008.
46. Lemke R.L., Zhong Z., Campbell C.A., Zentner R.P. Can pulse crops play a role in mitigating greenhouse gases from North American agriculture? Agron J., 2007, Vol. 99. P. 1719–25
47. Lesk C., Rowhani P., Ramankutty N. Influence of extreme weather disasters on global crop production. Nature, 2016, Vol. 529. P. 84–87
48. Li M., Li Z., Zhou S., Guo H., He X. and et al. Advances in the Root System Architecture Regulated by Plant Rhizosphere Microorganisms. Chinese Journal of Agrometeorology, 2021, Vol 42, Issue 11. P. 895-904. https://doi.org/10.3969/j.issn.1000-6362.2021.11.001; 49. Liao H., Rubio G., Yan X., Cao A., Brown K.M. & Lynch J.P. Effect of phosphorus availability on basal root shallowness in common bean. Plant and Soil, 2001, Vol. 232. P. 69–79 https://doi.org/10.1023/A:1010381919003.
50. Lima J.V., Tinôco R.S., Olivares F.L., Chia G.S., de Melo Júnior J.A.G. and da Silva G.B. Rhizobacteria modify root architecture and improve nutrient uptake in oil palm seedlings despite reduced fertilizer. Rhizosphere, 2021, Vol. 19. https://doi.org/10.1016/j.rhisph.2021.100420
51. Lin C., Sauter M. Control of adventitious root architecture in rice by darkness, light, and gravity. Plant Physiology, 2018, Vol. 176. P. 1352–1364. https://doi.org/10.1104/pp.17.01540.
52. Linkohr B.I., Williamson L.C., Fitter A.H., Leyser H.M.O. Nitrate and phosphate availability and distribution have different effects on root system architecture of Arabidopsis. The Plant Journal, 2002, Vol. 29. P. 751–760. https://doi.org/10.1046/j.1365-313x.2002.01251.x
53. Lobell D.B., Roberts M.J., Schlenker W.,
Braun N., Little B.B., and et al. Greater sensitivity to drought accompanies maize yield increase in the U.S. Midwest. Science, 2014, Vol. 344. P. 516–519.
54. López-Bucio J., Cruz-Ramírez A., Herrera-Estrella L. The role of nutrient availability in regulating root architecture. Current Opinion in Plant Biology, 2003, Vol. 6. P. 280–287 https://doi.org/10.1016/s1369-5266(03)00035-9.
55. Loudet O., Gaudon V., Trubuil A., Daniel-Vedele F. Quantitative trait loci controlling root growth and architecture in Arabidopsis thaliana confirmed by heterogeneous inbred family. Theoretical and Applied Genetics, 2005, Vol. 110. P. 742 –753. https://doi.org/10.1007/s00122-004-1900-9
56. Lynch J. Root architecture and plant productivity. Plant Physiol., 1995, Vol. 109. P. 7–13. https://doi.org/10.1104/pp.109.1.7
57. Lynch J. The Role of Nutrient-Efficient Crops in Modern Agriculture. Journal of Crop Production, 1998, Vol. 1. P. 241–264. https://doi.org/10.1300/J144v01n02_10.
58. Lynch J.P. Harnessing root architecture to address global challenges. The Plant Journal, 2022, Vol. 109. P. 415–431. https://doi.org/10.1111/tpj.15560.
59. Lynch J.P. Roots of the Second Green Revolution. Australian Journal of Botany, 2007, Vol. 55, Issue 5. P. 493-512. https://doi.org/10.1071/BT06118.
60. Lynch J.P. Steep, cheap and deep: an ideotype to optimize water and N acquisition by maize root systems. Annals of Botany 112: 347–357, 2013. doi:10.1093/aob/mcs293.
61. Lynch J.P. Root phenes for enhanced soil exploration and phosphorus acquisition: tools for future crops. Plant Physiology, 2011, Vol. 156. P. 1041–1049. https://doi.org/10.1104/pp.111.175414.
62. Lynch, J.P. Root phenotypes for improved nutrient capture: an underexploited opportunity for global agriculture. New Phytol., 2019, Vol. 223. P. 548–564. https://doi.org/10.1111/nph.15738.
63. Malamy J.E. Intrinsic and environmental response pathways that regulate root system architecture. Plant Cell Environ., 2005, Vol. 28, Issue 1. P. 67-77. https://doi.org/10.1111/j.1365-3040.2005.01306.x
64. Mantelin S., Desbrosses G., Larcher M., Tranbarger T.J., Cleyet-Marel J.C., and Touraine B. Nitrate-dependent control of root architecture and N nutrition are altered by a plant growth- promoting Phyllobacterium sp. Planta, 2006, Vol. 223. P. 591–603. https://doi.org/10.1007/s00425-005-0106-y
65. Martins M.S., de Brito G.G., da Conceição Gonçalves W., Tripode B.M.D., Lartaud M. and et al. PhenoRoots: an inexpensive non-invasive phenotyping system to assess the variability of the root system architecture. Genetics and Plant Breeding. Sci. agric. (Piracicaba, Braz.), 2020, Vol. 77, Issue 5. https://doi.org/10.1590/1678-992X-2018-0420
66. McGrail R.K., Van Sanford D.A. and McNear D.H. Trait-Based Root Phenotyping as a Necessary Tool for Crop Selection and Improvement. Jr. Agronomy, 2020, Vol. 10. P. 1328; https://doi.org/10.3390/agronomy10091328.
67. Ning Y., Xiao Z., Weinmann M., Li Z. Phosphate uptake is correlated with the root length of celery plants following the association between arbuscular mycorrhizal fungi, Pseudomonas sp. and biochar with different phosphate fertilization levels. Agronomy, 2019, Vol. 9. P. 824. https://dx.doi.org/10.3390/agronomy9120824.
68. Nosheen A., Bano A., Ullah F., Farooq U., Yasmin H., and Hussain I. Effect of plant growth promoting rhizobacteria on root morphology of Safflower (Carthamus tinctorius L.). Afr. J. Biotechnol., 2011, Vol. 10. P. 12639–12649. https://doi.org/10.5897/AJB11.1647.
69. Opitz N., Marcon C., Paschold A., Malik WA., Lithio A., and et al. 2016. Extensive tissuespecific transcriptomic plasticity in maize primary roots upon water deficit. Journal of Experimental Botany., 2016, Vol. 67. P. 1095–1107. https://doi. 10.1093/jxb/erv453
70. Paez-Garcia A., Motes C. M., Scheible W.-R., Chen R., Blancaflor E. B., Monteros M. J. Root traits and phenotyping strategies for plant improvement. Plants., 2015, Vol.4, Issue 2. P. 334–355. https://doi.10.3390/plants4020334.
71. Pagès L. Root system morphogenesis. Particular traits of trees. In: INRA (ed) Huitiemecolloque sur les recherches fruitières, “La racine – le porte-greffe. Centre Technique Interprofessionnel des Fruits et Legumes, Bordeaux. 1989. P. 81–92. URL: https://www.researchgate.net/publication/271529393_Root_system_Architecture.
72. Poorter H., Fiorani F., Pieruschka R., Wojciechowski T., van der Putten W.H., Kleyer M. et al. Pampered inside, pestered outside? differences and similarities between plants growing in controlled conditions and in the field. New Phytol., 2016, Vol. 212. P. 838–855. https://doi.10.1111/nph.14243.
73. Quan W., Liu X., Wang H., Chan Z. Comparative Physiological and Transcriptional Analyses of Two Contrasting Drought Tolerant Alfalfa Varieties. Front. Plant Sci., 2016. Vol. 6. P. 12-56 https://doi. org/10.3389/fpls.2015.01256.
74. Rattanapichai W., Klem K. Two-dimensional Root Phenotyping System Based on Root Growth on Black Filter Paper and Recirculation Micro-irrigation. Czech Journal of Genetics and Plant Breeding. 2016. Vol. 52, Issue 2. P.64-70. https://doi. 10.17221/121/2015-CJGPB.
75. Ray DK., Mueller ND., West PC, Foley JA. 2013. Yield trends are insufficient to double global crop production by 2050. Plos One. 2013. Vol. 8, Issue 2 : e66428.. https://doi. 10.1371/journal.pone.0066428
76. Rellan-Alvarez R., Lobet G., Lindner H., Pradier P.L., Sebastian J. and et al. GLO-Roots: an imaging platform enabling multidimensional characterization of soilgrown root systems. 2015. https://doi.10.7554/eLife.07597.
77. Rich S. M., Christopher J., Richards R., Watt M. Root phenotypes of young wheat plants grown in controlled environments show inconsistent correlation with mature root traits in the field. Journal of Experimental Botany. 2020. Vol. 71, Issue 16. P. 4751–4762. https://doi.10.1093/jxb/eraa201.
78. Rosenzweig C., Elliott J., Deryng D., Ruane A.S., Muller C. et al. Assessing agricultural risks of climate change in the 21st century in a global gridded crop model intercomparison. Proceedings of the National Academy of Sciences, USA. 2014. Vol. 111. P. 3268–3273. https://doi.org/10.21073/pnas1222463110.
79. Roumet C., Urcelay C., Diaz S. Suites of root traits differ between annual and perennial species growing in the field. New Phytol., 2006, Vol. 170. P. 357–368. https://doi.org/10.1111/j.1469-8137.2006.01667.x.
80. Schellenbaum L., Berta G., Ravolanirina F., Tisserant, B., Gianinazzi S., Fitter, A.H. Influence of endomycorrhizal infection on root morphology in a micropropagated woody plant species (Vitis vinifera L.). Ann. Bot., 1991, Vol. 68, P. 135-141.
81. Schneider H., Klein S., Hanlon M., Brown K., Kaeppler S. and Lynch J. Genetic control of root anatomical plasticity in maize. Plant Genome. 2020, Vol. 13, Issue 2. https://doi.org/10.1002/tpg2.20003.
82. Schneider H., Klein S., Hanlon M., Nord E., Kaeppler S., Brown K., et al. Genetic control of root architectural plasticity in maize. J. Exp. Bot., 2020, Vol. 71, Issue 10. P. 3185-3197. https://doi.org/10.1093/jxb/eraa084.
83. Sebastian J, Yee MC, Goudinho Viana W, et al. 2016. Grasses suppress shoot-borne roots to conserve water during drought. Proceedings of the National Academy of Sciences, USA., 2016, Vol. 113. P. 8861–8866. https://doi.org/10.1073/pnas.1604021113.
84. Shao H., Shi D., Shi W., et al. Genotypic difference in the plasticity of root system architecture of field-grown maize in response to plant density. Plant and Soil., 2019, Vol. 439, Issue 1-2. P. 201–217. https://doi.org/10.1007/s11104-019-03964-8
85. Sponchiado B.N., White J.W., Castillo J.A., Jones P.G. Root growth of four common bean cultivars in relation to drought tolerance in environments with contrasting soil types. Experimental Agriculture, 1989, Vol. 25. P. 249–257.
86. Teramoto S. and Uga Y. A deep learning-based phenotypic analysis of rice root distribution from field images. Plant phenomics, 2020, Vol. 2020, article 3194308. P. 1–10.
87. Teramoto S., Takayasu S., Kitomi Y., Arai-Sanoh Y., Tanabata T. and Uga Y. High-throughput threedimensional visualization of root system architecture of rice using X-ray computed tomography. Plant Methods, 2020, Vol. 16, No. 1.
88. Tjoelker M.G., Craine J.M., Wedin D., Reich P.B., Tilman D. Linking leaf and root trait syndromes among 39 grassland and savannah species. New Phytol., 2005, Vol. 167. P. 493–508. https://doi.org/10.1111/j.1469-8137.2005.01428.x
89. Trachsel S., Kaeppler S.M., Brown K.M. and Lynch J.P. Maize root growth angles become steeper under low N conditions. F. Crop. Res., 2013, Vol. 140. P. 18–31. https://doi.org/10.1016/j.fcr.2012.09.010.
90. Turan M., Arjumend T., Argın S., Yildirim E., Katırcıoğlu H. and et al. Plant Root Enhancement by Plant Growth Promoting Rhizobacteria. In book: Plant Roots / Edited by Yildirim E., Turan M. and Ekinci M. 2021. https://doi.org/10.5772/intechopen.99890.
91. Vance C.P., Uhde-Stone C., Allan D.L. Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytologist, 2003, Vol. 157. P. 423–447. https://doi.org/10.1046/j.1469-8137.2003.00695.x
92. Waines J.G., Ehdaie B. Domestic ation and crop physiology: roots of green-revolution wheat. Ann. Bot., 2007, Vol. 100. P. 991–998. https://doi.org/10.1093/aob/mcm180.
93. Waisel Y., Eshel A., Kafkafi U. Aeroponics: a tool for root research under minimal environmental restrictions. In: Plant roots: the hidden half, 2002, Vol. 3. P. 323–331.
94. White Ph.J., George T.S., Dupuy L.X., Karley A.J., Valentine T.A. and et al. Root traits for infertile soils. Front Plant Sci., 2013, Vol. 4. P. 93. https://doi.org/10.3389/fpls.2013.00193.
95. Williamson L.C., Ribrioux S.P.C.P., Fitter A.H., Leyser H.M.O. Phosphate availability regulates root system architecture in Arabidopsis. Plant Physiology, 2001, Vol. 126. P. 875–882. https://doi.org/10.1104/pp.126.2.875.
96. Xie Q., Fernando K.M.C., Mayes S., Sparkes D.L. Identifying seedling root architectural traits associated with yield and yield components in wheat. Annals of Botany, 2017, Vol. 119, Issue 7. P. 1115–1129. https://doi.org/10.1093/aob/mcx001.
97. Xu Z., York L.M., Seethepalli A., Bucciarelli B., Cheng H. and et al. Objective Phenotyping of Root System Architecture Using Image Augmentation and Machine Learning in Alfalfa (Medicago sativa L.). Plant Phenomics, 2022. 9879610. https://doi.org/10.34133/2022/9879610
98. Yadav S.S., Hunter D., Redden B., Nang M., Yadava D.K., Habibi A.B. Impact of climate change on agriculture production, food, and nutritional security. In: Redden R., et al. Crop wild relatives and climate change. New Jersey, USA: Wiley, 2015. P. 1–23
99. Ye H., Roorkiwal M., Valliyodan B., Zhou L., Chen P. et al. Genetic diversity of root system architecture in response to drought stress in grain legumes. Journal of Experimental Botany, 2018, Vol. 69, No. 13. P. 3267–3277. https://doi.org/doi:10.1093/jxb/ery082
100. Yi K., Li X., Chen D., Yang S., Liu Y. et al. Root Spatial Distribution Induced by Phosphorus Deficiency Contributes to Topsoil Foraging and Low Phosphorus Adaption in Sugarcane (Saccharum officinarum L.). Front. Plant Sci., 2022, Vol. 12. https://doi.org/10.3389/fpls.2021.797635.
101. Yu L., Zhang H., Zhang W., Han B., Zhou H. et al. Arbuscular Mycorrhizal Fungi Alter the Interaction Effects Between Bacillus and Rhizobium on Root Morphological Traits of Medicago ruthenica L. Journal of Soil Science and Plant Nutrition, 2023, Vol. 23, Issue 2. P. 2868-2877. https://doi.org/10.1007/s42729-023-01242-2.
102. Zhang Y., Ma Y., Zhao D., Tang Z, Zhang T. et al. Genetic regulation of lateral root development. Plant Signal Behav., 2023, Vol. 18, Issue 1.:2081397. https://doi.org/10.1080/15592324.2022.2081397.
103. Zhaо J., Bodner G., Rewald B., Leitner D., Nagel K.A., Nakhforoosh A. Root architecture simulation improves the inference from seedling root phenotyping towards mature root systems. Journal of Experimental Botany, 2017, Vol. 68, No. 5. P. 965–982. https://doi.org/10.1093/jxb/erw494 A.
104. Zhensong Li, Xianglin Li and Feng He. Drip Irrigation Depth Alters Root Morphology and Architecture and Cold Resistance of Alfalfa. Agronomy, 2022, Vol. 12. P. 2192. https://doi.org/ 10.3390/agronomy12092192.
105. Zhu J., Ingram P. A., Benfey P. N., Elich T. From lab to field, new approaches to phenotyping root system architecture. Current Opinion in Plant Biology, 2011, Vol. 14, Issue 3. P. 310–317. https://doi.org/10.1016/j.pbi.2011.03.020.
106. Zou Y.N., Wu Q.S., Li Y., Huang Y.M. Effects of arbuscular mycorrhizal fungi on root system morphology and sucrose and glucose contents of Poncirus trifoliata. Chinese Journal of Applied Ecology, 2014, Vol. 25, Issue 4. P. 1125-1129.
Published
2024-03-20
Section
BREEDING, SEED PRODUCTION