Regulation of root morphogenesis in arbuscular mycorrhizae: What role do fungal exudates, phosphate, sugars and hormones play in lateral root formation?

Annals of Botany

Volumn 113, Issue 1, 2014, Pages 19-33

  Fusconi, Anna ^a  

^a UNIVERSITY OF TURIN   (Italy)

Author keywords

Arabidopsis thaliana; Arbuscular mycorrhizae; auxin; cytokinins; ethylene; fungal exudates; lateral roots; phosphate; root branching; strigolactones; sugars

Indexed keywords

ARBUSCULAR MYCORRHIZA; BIOMASS; CARBOHYDRATE; ETHYLENE; FUNGUS; GROWTH RESPONSE; HORMONE; MORPHOGENESIS; PHOSPHATE; PHYSIOLOGY; ROOT COLONIZATION; SUGAR;

AUXIN; CARBOHYDRATE; CYTOKININ; ETHYLENE; ETHYLENE DERIVATIVE; PHOSPHATE; PHYTOHORMONE;

ARABIDOPSIS; ARABIDOPSIS THALIANA; ARBUSCULAR MYCORRHIZAE; BIOAVAILABILITY; CARBOHYDRATE METABOLISM; EXUDATE; FUNGAL EXUDATES; LATERAL ROOTS; METABOLISM; MICROBIOLOGY; MYCORRHIZA; PHYSIOLOGY; PLANT ROOT; REVIEW; ROOT BRANCHING; SIGNAL TRANSDUCTION; STRIGOLACTONES;

ARABIDOPSIS THALIANA; ARBUSCULAR MYCORRHIZAE; AUXIN; CYTOKININS; ETHYLENE; FUNGAL EXUDATES; LATERAL ROOTS; PHOSPHATE; ROOT BRANCHING; STRIGOLACTONES; SUGARS;

ARABIDOPSIS; BIOLOGICAL AVAILABILITY; CARBOHYDRATE METABOLISM; CARBOHYDRATES; ETHYLENES; EXUDATES AND TRANSUDATES; MYCORRHIZAE; PHOSPHATES; PLANT GROWTH REGULATORS; PLANT ROOTS; SIGNAL TRANSDUCTION;

EID: 84891502994     PISSN: 03057364     EISSN: 10958290     Source Type: Journal    
DOI: 10.1093/aob/mct258     Document Type: Review

References (178)

1. Abdel-Lateif K, Bogusz D, Hocher V. 2012. The role of flavonoids in the establishment of plant roots endosymbioses with arbuscular mycorrhiza fungi, rhizobia and Frankia bacteria. Plant Signaling and Behavior 7: 1-6
2. Akhtar MS, Oki Y, Adachi T. 2009. Mobilization and acquisition of sparingly soluble P-sources by Brassica cultivars under P-starved environment. II. Rhizospheric pH changes, redesigned root architecture and Pi-uptake kinetics. Journal of Integrative Plant Biology 51: 1024-1039
3. Akiyama K, Matsuzaki K, Hayashi H. 2005. Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435: 824-827
4. Allen MF, Moore TS Jr, Christensen M. 1980. Phytohormone changes in Bouteloua gracilis infected by vesicular-Arbuscular mycorrhizae. I. Cytokinin increases in the host plant. Canadian Journal of Botany 58: 371-374
5. Aloni R, Aloni E, Langhans M, Ullrich CI. 2006.Role of cytokinin and auxin in shaping root architecture: Regulating vascular differentiation, lateral root initiation, root apical dominance and root gravitropism. Annals of Botany 97: 883-893
6. Aalsteinsson S, JensénP. 1989. Modifications of root geometry in winter wheat by phosphorus deprivation. Journal of Plant Physiology 135: 513-517
7. Aalsteinsson S, Jensén P. 1990. Influence of temperature on root development and phosphate influx in winter wheat grownat differentPlevels. Physiologia Plantarum 80: 69-74
8. Anurada M, Narayanan A. 1991. Promotion of root elongation by phosphorus deficiency. Plant and Soil 136: 273-275
9. Arata Y, Nagasawa-Iida A, Uneme H, Nakajima H, Kakimoto T, Sato R. 2010. The phenylquinazoline compound S-4893 a non-competitive cytokinin antagonist that targets Arabidopsis cytokinin receptor CRE1 and promotes root growth in Arabidopsis and rice. Plant and Cell Physiology 51: 2047-2059
10. Arite T, Umehara M, Ishikawa S, et al. 2009. d14, a strigolactone- insensitive mutant of rice, shows an accelerated outgrowth of tillers. Plant and Cell Physiology 50: 1416-1424
11. Arite T, Kameoka H, Kyozuka J. 2012. Strigolactone positively controls crown root elongation in rice. Journal of Plant Growth Regulation 31: 165-172
12. Baas R, Kuiper D. 1989. Effects of vesicular-Arbuscular mycorrhizal infection and phosphate on Plantago major ssp. pleiosperma in relation to internal cytokinin concentration. Physiologia Plantarum 76: 211-215
13. Balzergue C, Puech-PagèsV, Bécard G, RochangeSF. 2011. The regulation of arbuscular mycorrhizal symbiosis by phosphate in pea involves early and systemic signaling events. Journal of Experimental Botany 62: 1049-1060
14. Barea JM, Azcón-Aguilar C. 1982. Production of plant growth-regulating substances by the vesicular-Arbuscular mycorrhizal fungus Glomus mosseae. Applied and Environmental Microbiology 43: 810-813
15. Barker SJ, Tagu D. 2000. The roles of auxins and cytokinins in mycorrhizal symbioses. Journal of Plant Growth Regulation 19: 144-154
16. Bennett T, Sieberer T, Willett B, Booker J, Luschnig C, Leyser O. 2006. The Arabidopsis MAX pathway controls shoot branching by regulating auxin transport. Current Biology 16: 553-563
17. Berta G, Fusconi A, Trotta A, Scannerini S. 1990. Morphogenetic modifications induced by the mycorrhizal fungus Glomus strain E3 in the root system of Allium porrum L. New Phytologist 114: 207-215
18. Berta G, Fusconi A, Trotta A. 1993. VA mycorrhizal infection and the morphology and function of root systems. Environmental and Experimental Botany 33: 159-173
19. Berta G, Trotta A, Fusconi A, et al. 1995. Arbuscular mycorrhizal induced changes to plant growth and root system morphology in Prunus cerasifera. Tree Physiology 15: 281-293
20. Berta G, Sampò S, Gamalero E, Massa N, Lemanceau P. 2005. Suppression of Rhizoctonia root-rot of tomato by Glomus mossae BEG12 and Pseudomonas fluorescens A6RI is associated with their effect on the pathogen growth and on the root morphogenesis. European Journal of Plant Pathology 111: 279-288
21. Besmer YL, KoideRT. 1999. Effect of mycorrhizal colonization and phosphorous on ethylene production by snapdragon (Anthirrhinummajus L) flowers. Mycorrhiza 9: 161-166
22. Besserer A, Puech-Pagès V, Kiefer P, et al. 2006. Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biology 4: E226
23. Bielach A, Podlešáková K, Marhavý P, et al. 2012.Spatiotemporal regulation of lateral root organogenesis in Arabidopsis by cytokinin. The Plant Cell 24: 3967-3981
24. Bonfante P, Requena N. 2011. Dating in the dark: How roots respond to fungal signals to establish arbuscular mycorrhizal symbiosis. Current Opinion in Plant Biology 14: 451-457
25. Borch K, Bouma TJ, Lynch JP, Brown KM.1999. Ethylene: A regulator of root architectural responses to soil phosphorus availability. Plant, Cell and Environment 22: 425-431
26. Branscheid A, Sieh D, Pant BD, et al. 2010. Expression pattern suggests a role of MiR399 in the regulation of the cellular response to local Pi increase during arbuscular mycorrhizal symbiosis. Molecular Plant-Microbe Interactions 23: 915-926
27. Brewer PB, Koltai H, Beveridge CA. 2013. Diverse roles of strigolactones in plant development. Molecular Plant 6: 18-28
28. Calcagno C, Novero M, Genre A, Bonfante P, Lanfranco L. 2012. The exudate froman arbuscular mycorrhizal fungus induces nitric oxide accumulation in Medicago truncatula roots. Mycorrhiza 22: 259-269
29. Catoira R, Galera C, de Billy F, et al. 2000. Four genes of Medicago truncatula controlling components of a Nod-factor transduction pathway. The Plant Cell 12: 1647-1665
30. Chen YH, Kao CH. 2012. Calcium is involved in oxide-And auxin-induced lateral root formation in rice. Protoplasma 249: 187-195
31. Chen ZH, Nimmo GA, Jenkins GI, Nimmo HG. 2007. BHLH32 modulates several biochemical and morphological processes that respond to Pi starvation in Arabidopsis. Biochemical Journal 405: 191-198
32. Chiou TJ, Lin SI. 2011. Signaling network in sensing phosphate availability in plants. Annual Review of Plant Biology 62: 185-206
33. Ciereszko I, Zambryzcka A, Rychter A. 1998. Sucrose hydrolysis in bean roots (Phaseolus vulgaris L) under phosphate deficiency. Plant Science 133: 139-144
34. Ciereszko I, Johansson H, Hurry V, Kleczkowski LA. 2001. Phosphate status affects the gene expression, protein content and enzymatic activity of UDP-glucose pyrophosphorylase in wildtype and pho mutants of Arabidopsis. Planta 212: 598-605
35. Citernesi AS, Vitagliano C, GiovannettiM.1998. Plant growth and root system morphologyof Olea europaea L. rooted cuttings as influenced byarbuscular mycorrhizas. Journal of Horticultural Science and Biotechnology 73: 647-654
36. Cook CE, Whichard LP, Turner B, Wall ME, Grant H. 1966. Germination of witchweed (Striga lutea Lour): Isolation and properties of a potent stimulant. Science 154: 1189-1190
37. Dai X, Wang Y, Yang A, Zhang WH. 2012. OsMYB2P-1, an R2R3 MYB transcription factor, is involved in the regulation of phosphate-starvation responses and root architecture in rice. Plant Physiology 159: 169-183
38. Danneberg G, Latus C, Zimmer W, Hundeshagen B, Schneider-Poetsch H, Bothe H. 1992. Influence of vesicular-Arbuscular mycorrhiza on phytohormone balance in maize (Zea mays L). Journal of Plant Physiology 141: 33-39
39. Debi BR, Taketa S, Ichii M. 2005. Cytokinin inhibits lateral root initiation but stimulates lateral root elongation in rice (Oryza sativa). Journal of Plant Physiology 162: 507-515
40. DeMars BG, Boerner EJ. 1996.Vesicular arbuscular mycorrhizal development in the Brassicaceae in relation to plant life span. Flora 191: 179-189
41. De Smet I. 2011. Lateral root initiation: One step at a time. New Phytologist 193: 867-873
42. Devaiah BN, Madhuvanthi R, Karthikeyan AS, Raghothama KG. 2009. Phosphate starvation responses and gibberellic acid biosynthesis are regulated by the MYB62 transcription factor in Arabidopsis. Molecular Plant 2: 43-58
43. Dinh PTY, Roldan M, Leung S, McManus MT. 2012. Regulation of root growth by auxin and ethylene is influenced by phosphate supply in white clover (Trifolium repens L). Plant Growth Regulation 66: 179-190
44. Drew MC. 1975. Comparison of the effects of a localized supply of phosphate, nitrate, ammonium and potassium on the growth of the seminal root system, and the shoot, in barley. New Phytologist 75: 479-490
45. Drüge U, SchönbeckF. 1992. Effects of vesicular-Arbuscular mycorrhizal infection on transpiration, photosynthesis and growth of flax (Linum usitatissimum L) in relation to cytokinin levels. Journal of Plant Physiology 141: 40-48
46. Dubrovsky JG, Napsucialy-Mendivil S, Duclercq J, et al. 2011. Auxin minimum defines a developmental window for lateral root initiation. New Phytologist 191: 970-983
47. Dugassa GD, von Alten H, Schönbeck F. 1996. Effects of arbuscular mycorrhiza (AM) on health of Linum usitatissimum L. infected by fungal pathogens. Plant and Soil 185: 173-182
48. Feddermann N, Finlay R, Boller T, Elfstrand M. 2010. Functional diversity in arbuscular mycorrhiza-The role of gene expression, phosphorus nutrition and symbiotic efficiency. Fungal Ecology 3: 1-8
49. Finet C, Jaillais Y. 2012. Auxology: When auxin meets plant evo-devo. Developmental Biology 369: 19-31
50. Fiorilli V, Catoni M, Mozzi L, Novero M, Accotto GP, Lanfranco L. 2009. Global and cell-Type gene expression profiles in tomato plants colonized by an arbuscular mycorrhizal fungus. New Phytologist 184: 975-987
51. FitterAH.2006.What is the link between carbon and phosphorus fluxes in arbuscular mycorrhizas? A null hypothesis for symbiotic function. New Phytologist 172: 3-6
52. Fitze D, Wiepninga A, Kaldorf M, Ludwig-Müller J. 2005. Auxins in the development of an arbuscular mycorrhizal symbiosis in maize. Journal of Plant Physiology 162: 1210-1219
53. Foo E, Ross JJ, Jones WT, Reid JB. 2013. Plant hormones in arbuscular mycorrhizal symbioses: An emerging role for gibberellins. Annals of Botany 111: 769-779
54. Forde B, Lorenzo H. 2001. The nutritional control of root development. Plant and Soil 232: 51-68
55. Formey D, Jourda C, Roux C, Delaux PM. 2013. What the genomics of arbuscular mycorrhizal symbiosis teaches us about root development. In: Crespi M, ed. Root genomics and soil interactions. Oxford: Blackwell, 171-188
56. Franco-Zorrilla JM, Martin AC, Solano R, Rubio V, Leyva A, Paz-Ares J. 2002. Mutations at CRE1 impair cytokinin-induced repression of phosphate starvation responses in Arabidopsis. The Plant Journal 32: 353-60
57. Fukaki H, Tasaka M. 2009. Hormone interactions during lateral root formation. Plant Molecular Biology 69: 437-449
58. Gamalero E, Berta G, Massa N, Glick BR, Lingua G. 2008. Synergistic interactions between the ACC deaminase-producing bacterium Pseudomonas putida UW4 and the AM fungus Gigaspora rosea positively affect cucumber plant growth. FEMS Microbiology Ecology 64: 459-467
59. Genre A, Chabaud M, Balzergue C, et al. 2013. Short-chain chitin oligomers from arbuscular mycorrhizal fungi trigger nuclear Ca2+ spiking in Medicago truncatula roots and their production is enhanced by strigolactone. New Phytologist 198: 190-202
60. Gonzalez-Rizzo S, Crespi M, Frugier F. 2006. The Medicago truncatula CRE1 cytokinin receptor regulates lateral root development and early symbiotic interaction with Sinorhizobium meliloti. The Plant Cell 18: 2680-2693
61. Gou J, Strauss SH, Tsai CJ, et al. 2010. Gibberellins regulate lateral root formation in Populus through interactions with auxin and other hormones. The Plant Cell 22: 623-639
62. Grace EJ, Cotsaftis O, Tester M, Smith FA, Smith SE. 2009. Arbuscular mycorrhizal inhibition of growth in barley cannot be attributed to extent of colonization, fungal phosphorus uptake or effects on expression of plant phosphate transporter genes. New Phytologist 181: 938-949
63. Gutjahr C, Casieri L, Paszkowski U. 2009a. Glomus intraradices induces changes in root system architecture of rice independently of common symbiosis signaling. New Phytologist 182: 829-837
64. Gutjahr C, Novero M, Guether M, Montanari O, Udvardi M, Bonfante P. 2009b. Presymbiotic factors released by the arbuscular mycorrhizal fungus Gigaspora margarita induce starch accumulation in Lotus japonicus roots. New Phytologist 183: 53-61
65. Hammond JP, White PJ. 2008. Sucrose transport in the phloem: Integrating root responses to phosphorus starvation. Journal of Experimental Botany 59: 93-109
66. Hammond JP, White PJ. 2011. Sugar signaling in root responses to low phosphorus availability. Plant Physiology 156: 1033-1040
67. Hanlon MT, Coenen C. 2011. Genetic evidence for auxin involvement in arbuscular mycorrhiza initiation. New Phytologist 189: 701-709
68. Harrison MJ. 2005. Signaling in the arbuscular mycorrhizal symbiosis. Annual Review of Microbiology 59: 19-42
69. Harrison M, Dixon R. 1994. Spatial patterns of expression of flavonoid/isoflavonoid pathway genes during interactions between roots of Medicago truncatula and the mycorrhizal fungus Glomus versiforme. The Plant Journal 6: 9-20
70. Hause B, Mrosk C, Isayenkov S, Strack D. 2007. Jasmonates in arbuscular mycorrhizal interactions. Phytochemistry 68: 101-110
71. Helber N, Wippel K, Sauer N, Schaarschmidt S, Hause B, Requena N. 2011. A versatile monosaccharide transporter that operates in the arbuscular mycorrhizal fungus Glomus sp is crucial for the symbiotic relationship with plants. The Plant Cell 23: 3812-3823
72. Hermans C, Hammond JP, White PJ, Verbruggen N. 2006. How do plants respond to nutrient shortage by biomass allocatioñ Trends in Plant Science 11: 610-617
73. Hodge A, Berta G, Doussan C, Merchan F, Crespi M. 2009. Plant root growth, architecture and function. Plant and Soil 321: 153-187
74. Hooker JE, Munro M, Atkinson D. 1992. Vesicular-Arbuscular mycorrhizal fungi induced alteration in poplar root system morphology. Plant and Soil 145: 207-214
75. Ivanchenko MG, Muday GK, Dubrovsky JG. 2008. Ethylene-Auxin interactions regulate lateral root initiation and emergence in Arabidopsis thaliana. The Plant Journal 5: 335-347
76. Jain A, Poling MD, Karthikeyan AS, et al. 2007. Differential effects of sucrose and auxin on localized phosphate deficiency-induced modulation of different traits of root system architecture in Arabidopsis. Plant Physiology 144: 232-247
77. Janssen BJ, Snowden KC. 2012. Strigolactone and karrikin signal perception: Receptors, enzymes, or both? Frontiers in Plant Science/Plant Evolution and Development 3: 1-13
78. Jentschel K, Thiel D, Rehn F, Ludwig-Müller J. 2007. Arbuscular mycorrhiza enhances auxin levels and alters auxin biosynthesis in Tropaeolum majus during early stages of colonization. Physiologia Plantarum 129: 320-333
79. Jiang C, Gao X, Liao L, Harberd NP, Fu X. 2007. Phosphate starvation root architecture and anthocyanin accumulation responses are modulated by the gibberellin-DELLA signaling pathway in Arabidopsis. Plant Physiology 145: 1460-1470
80. Jones B, Ljung K. 2012. Subterranean space exploration: The development of root system architecture. Current Opinion in Plant Biology 15: 97-102
81. Kaldorf M, Ludwig-Müller J. 2000. AM fungi might affect the root morphology of maize by increasing indole-3-butyric acid biosynthesis. Physiologia Plantarum 109: 58-67
82. Kapulnik Y, Delaux PM, Resnick N, et al. 2011a. Strigolactones affect lateral root formation and root-hair elongation in Arabidopsis. Planta 233: 209-216
83. Kapulnik Y, Resnick N, Mayzlish-Gati E, et al. 2011b. Strigolactones interact with ethylene and auxin in regulating root-hair elongation in Arabidopsis. Journal of Experimental Botany 62: 2915-2924
84. Karthikeyan AS, Varadarajan DK, Jain A, Held MA, Carpita NC, Raghothama KG. 2007. Phosphate starvation responses are mediated by sugar signaling in Arabidopsis. Planta 225: 907-918
85. Kiers ET, Duhamel M, Beesetty Y, et al. 2011. Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333: 880-882
86. Kohlen W, Charnikhova T, Liu Q. 2011. Strigolactones are transported through the xylem and play a key role in shoot architectural response to phosphate deficiency in nonarbuscular mycorrhizal host Arabidopsis. Plant Physiology 155: 974-987
87. Koltai H, Dor E, Hershenhorn J, et al. 2010. Strigolactoneś effect on root growth and root-hair elongation may be mediated by auxin-efflux carriers. Journal of Plant Growth Regulation 29: 129-136
88. Koltai H. 2013. Strigolactones activate different hormonal pathways for regulation of root development in response to phosphate growth conditions. Annals of Botany 112: 409-415
89. Kuppusamy KT, Ivashuta S, Bucciarelli B, et al. 2009. Knockdown of CELL DIVISION CYCLE16 reveals an inverse relationship between lateral root and nodule numbers and a link to auxin in Medicago truncatula. Plant Physiology 151: 1155-1166
90. Laplaze L, Benkova E, Casimiro I, et al. 2007. Cytokinins act directly on lateral root founder cells to inhibit root initiation. The Plant Cell 19: 3889-3900
91. Lei M, Zhu C, Liu Y, et al. 2010. Ethylene signalling is involved in regulation of phosphate starvation-induced gene expression and production of acid phosphatases and anthocyanin in Arabidopsis. New Phytologist 189: 1084-1095
92. Lei M, Liu Y, Zhang B, et al. 2011. Genetic and genomic evidence that sucrose is a global regulator of plant responses to phosphate starvation in Arabidopsis. Plant Physiology 156: 1116-1130
93. Lewis DR, Negi S, Sukumar P, Muday GK. 2011. Ethylene inhibits lateral root development, increases IAA transport and expression of PIN3 and PIN7 auxin efflux carriers. Development 138: 3485-3495
94. Li YS, Mao XT, Tian QY, Li LH, Zhang WH. 2009. Phosphorus deficiency-induced reduction in root hydraulic conductivity in Medicago falcata is associated with ethylene production. Environmental and Experimental Botany 67: 172-177
95. Li Z, Xu C, Li K, Yan S, Qu X, Zhang J. 2012. Phosphate starvation of maize inhibits lateral root formation and alters gene expression in the lateral root primordium zone. BMC Plant Biology 12: 89-105
96. Liu W, Kohlen W, Lillo A. 2011. Strigolactone biosynthesis in Medicago truncatula and rice requires the symbiotic GRAS-Type transcription factors NSP1 and NSP2. The Plant Cell 23: 3853-3865
97. López-Bucio J, Hernández-Abreu E, Sánchez- Calderón L, Nieto-Jacobo MF, Simpson J, Herrera-Estrella L. 2002. Phosphate availability alters architecture and causes changes in hormone sensitivity in the Arabidopsis root system. Plant Physiology 129: 244-256
98. López-Ráez JA, Verhage A, Fernández I. 2010. Hormonal and transcriptional profiles highlight common and differential host responses to arbuscular mycorrhizal fungi and the regulation of the oxylipin pathway. Journal of Experimental Botany 61: 2589-2601
99. López-Ráez JA, Charnikhova T, Fernández I, Bouwmeester H, Pozo MJ. 2011. Arbuscular mycorrhizal symbiosis decreases strigolactone production in tomato. Journal of Plant Physiology 168: 294-297
100. Ludwig-Müller J. 2010. Hormonal responses in host plants triggered by arbuscular mycorrhizal fungi. In: Koltai H, Kapulnik Y, eds. Arbuscular mycorrhizas: Physiology and function, 2nd edn. Dordrecht: Springer, 169-190
101. Ludwig-Müller J. 2011. Auxin conjugates: Their role for plant development and in the evolution of land plants. Journal of Experimental Botany 62: 1757-1773
102. Ludwig-Müller J, Güther M. 2007. Auxins as signals in arbuscular mycorrhiza formation. Plant Signaling and Behavior 2: 194-196
103. Lynch JP, Brown KM. 2001. Topsoil foraging-An architectural adaptation of plants to low phosphorus availability. Plant and Soil 237: 225-237
104. Ma Z, Baskin TI, Brown KM, Lynch JP. 2003. Regulation of root elongation under phosphorus stress involves changes in ethylene responsiveness. Plant Physiology 131: 1381-1390
105. MacGregor DR, Deak KI, Ingram PA, Malamy JE. 2008. Root system architecture in Arabidopsis grown in culture is regulated by sucrose uptake in the aerial tissues. The Plant Cell 20: 2643-2660
106. Maillet F, Poinsot V, André O, et al. 2011. Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469: 58-63
107. Marhavý P, Bielach A, Abas L, et al. 2011. Cytokinin modulates endocytic trafficking of PIN1 auxin efflux carrier to control plant organogenesis. Developmental Cell 21: 796-804
108. Martín-Rodríguez JA, León-Morcillo R, Vierheilig H, Ocampo JA, Ludwig-Müller J, García-Garrido JM. 2011. Ethylene-dependent/ ethylene-independentABAregulation of tomato plants colonized by arbuscular mycorrhiza fungi. New Phytologist 190: 193-205
109. Mayzlish-Gati E, De Cuyper C, Goormachtig S, et al. 2012. Strigolactones are involved in root response to lowphosphate conditions in Arabidopsis. Plant Physiology 160: 1329-1341
110. McArthur DAJ, Knowles NR. 1992. Resistance responses of potato to vesicular-Arbuscular mycorrhizal fungi under varying abiotic phosphorus levels. Plant Physiology 100: 341-351
111. Meixner C, Ludwig-Müller J, Miersch O, Gresshoff P, Staehelin C, Vierheilig H. 2005.Lackof mycorrhizal autoregulation and phytohormonal changes in the supernodulating soybean mutant nts1007. Planta 222: 709-715
112. Miura K, Rus A, Sharkhuu A, et al. 2005. The Arabidopsis SUMO E3 ligase SIZ1 controls phosphate deficiency responses. Proceedings of the National Academy of Sciences, USA 102: 7760-7765
113. Miura K, Lee J, Gong Q, et al. 2011. SIZ1 regulation of phosphate starvation-induced root architecture remodeling involves the control of auxin accumulation. Plant Physiology 155: 1000-1012
114. Mollier A, Pellerin S. 1999. Maize root system growth and development as influenced by phosphorus deficiency. Journal of Experimental Botany 50: 487-497
115. Muday GK, Rahman A, Binder BM. 2012. Auxin and ethylene: Collaborators or competitors? Trends in Plant Science 17: 181-195
116. Mukherjee A, Ané JM. 2011. Germinating spore exudates from arbuscular mycorrhizal fungi: Molecular and developmental responses in plants and their regulation by ethylene. Molecular Plant-Microbe Interactions 24: 260-270
117. Nacry P, Canivenc G, Muller B, et al. 2005.Arole for auxin redistribution in the responses of the root system architecture to phosphate starvation in Arabidopsis. Plant Physiology 138: 2061-2074
118. Nagarajan VK, SmithAP. 2012. Ethylenés role in phosphate starvation signaling: More than just a root growth regulator. Plant and Cell Physiology 53: 277-286
119. Negi S, Sukumar P, Liu X, Cohen JD, Muday GK. 2010. Genetic dissection of the role of ethylene in regulating auxin-dependent lateral and adventitious root formation in tomato. The Plant Journal 61: 3-15
120. Niu YF, Chai RS, Jin GL, Wang H, Tang CX, Zhang YS. 2013. Responses of root architecture development to low phosphorous availability: A review. Annals of Botany 112: 391-408
121. Oláh B, Brière C, Bécard G, Dénarié J, Gough C. 2005. Nod factors and a diffusible factor from arbuscular mycorrhizal fungi stimulate lateral root formation in Medicago truncatula via the DMI1/DMI2 signalling pathway. The Plant Journal 44: 195-207
122. Ortu G, Balestrini R, Pereira PA, Becker J, Küster H, BonfanteP. 2012. Plant genes related to gibberellin biosynthesis and signaling are differentially regulated during the early stages of AM fungal interactions. Molecular Plant 5: 951-954
123. Overvoorde P, Fukaki H, Beeckman T. 2010. Auxin control of root development. Cold Spring Harbor Perspectives in Biology 2: A001537
124. Pant BD, Buhtz A, Kehr J, Scheible WR. 2008. MicroRNA399 is a longdistance signal for the regulation of plant phosphate homeostasis. The Plant Journal 53: 731-738
125. Paszkowski U, BollerT. 2002. The growth defect of lrt1, a maize mutant lacking lateral roots, can be complemented by symbiotic fungi or high phosphate nutrition. Planta 214: 584-590
126. Péret B, De Rybel B, Casimiro I, et al. 2009. Arabidopsis lateral root development: An emerging story. Trends in Plant Sciences 14: 399-408
127. Péret B, Clément M, Nussaume L, Desnos T. 2011. Root developmental adaptation to phosphate starvation: Better safe than sorry. Trends in Plant Science 16: 442-450
128. Pérez-Torres CA, López-Bucio J, Cruz-Ramírez A, et al. 2008. Phosphate availability alters lateral root development in Arabidopsis by modulating auxin sensitivity via a mechanism involving the TIR1 auxin receptor. The Plant Cell 20: 3258-3272
129. Pierik R, Tholen D, Poorter H, Visser EJW, Voesenek LACJ. 2006. The Janus face of ethylene: Growth inhibition and stimulation. Trends in Plant Science 11: 176-183
130. Price NS, Roncadori RW, Hussey RS. 1989. Cotton root growth as influenced by phosphorus nutrition and vesicular-Arbuscular mycorrhizas. New Phytologist 111: 61-66
131. Puig J, Pauluzzi G, Guiderdoni E, GantetP. 2012.Regulation of shoot and root development through mutual signalling. Molecular Plant 5: 974-983
132. Quint M, Barkawi LS, Fan KT, Cohen JD, Gray WM.2009. Arabidopsis IAR4 modulates auxin response by regulating auxin homeostasis. Plant Physiology 150: 748-758
133. Ramaekers L, Remans R, Rao IM, Blair MW, Vanderleydena J. 2010. Strategies for improving phosphorus acquisition efficiency of crop plants. Field Crops Research 117: 169-176
134. Richter GL, Monshausen GB, Krol A, Gilroy S. 2009. Mechanical stimuli modulate lateral root organogenesis. Plant Physiology 151: 1855-1866
135. Rouached H, Arpat AB, Poirier Y. 2010. Regulation of phosphate starvation responses in plants: Signaling players and cross-Talks. Molecular Plant 3: 288-299
136. Rouached H, Stefanovic A, Secco D, et al. 2011. Uncoupling phosphate deficiency fromits major effects on growth and transcriptome viaPHO1expression in Arabidopsis. The Plant Journal 65: 557-570
137. Rubio V, Linhares F, Solano R, et al. 2001. A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Genes and Development 15: 2122-2133
138. Ruyter-Spira C, Kohlen W, Charnikhova T, et al. 2011. Physiological effects of the synthetic strigolactone analog GR24 on root system architecture in Arabidopsis: Another belowground role for strigolactones? Plant Physiology 155: 721-734
139. Sakakibara H. 2006. Cytokinins: Activity, biosynthesis, and translocation. Annual Review of Plant Biology 57: 431-449
140. Salama AMS, Wareing PF. 1979. Effects of mineral nutrition on endogenous cytokinins in plants of sunflower (Helianthus annuus L). Journal of Experimental Botany 30: 971-981
141. Sánchez-Calderón L, López-Bucio J, Chachón-López A, et al. 2005. Phosphate starvation induces a determinate developmental program in the roots of Arabidopsis thaliana. Plant and Cell Physiology 46: 174-184
142. Sato A, MiuraK. 2011.Root architecture remodeling induced by phosphate starvation. Plant Signaling and Behavior 6: 1122-1126
143. Scannerini S, Fusconi A, Mucciarelli M. 2001. The effect of endophytic fungi on host plant morphogenesis. In: Seckback J, ed. Symbiosis: Organisms and model systems. Dordrecht: Kluwer, 427-447
144. Schellenbaum L, Berta G, Raviolanirina F, Tisserant B, Gianinazzi S, Fitter AH. 1991. Influence of endomycorrhizal infection on root morphology in a micropropagated woody plant species (Vitis vinifera L). Annals of Botany 68: 135-141
145. Seto Y, Kameoka H, Yamaguchi S, Kyozuka J. 2012. Recent advances in strigolactone research: Chemical and biological aspects. Plant and Cell Physiology 53: 1843-1853
146. Shaul-Keinan O, Gadkar V, Ginzberg I, et al. 2002. Hormone concentrations in tobacco roots change during arbuscular mycorrhizal colonization with Glomus intraradices. New Phytologist 154: 501-507
147. Shkolnik-Inbar D, Bar-Zvi D. 2010. ABI4 mediates abscisic acid and cytokinin inhibition of lateral root formation by reducing polar auxin transport in Arabidopsis. The Plant Cell 22: 3560-3573
148. Simon S, Petrášek J. 2011. Why plants need more than one type of auxin. Plant Science 180: 454-460
149. Smith S, De Smet I. 2012. Root system architecture: Insights from Arabidopsis and cereal crops. Philosophical Transactions of the Royal Society B: Biological Sciences 367: 1441-1452
150. Smith SE, Read DJ. 2008. Mycorrhizal symbiosis, 3rd edn. London: Academic Press
151. Smith SE, Smith FA. 2012. Fresh perspectives on the roles of arbuscular mycorrhizal fungi in plant nutrition and growth. Mycologia 104: 1-13
152. Smith SE, Jakobsen I, Grønlund M, Smith FA. 2011. Roles of arbuscular mycorrhizas in plant phosphorus nutrition: Interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiology 156: 1050-1057
153. Smith SE, Smith FA. 2011. Roles of arbuscular mycorrhizas in plant nutrition and growth: New paradigms from cellular to ecosystem scales. Annual Review of Plant Biology 62: 227-250
154. Stepanova AN, Yun J, Likhacheva AV, Alonso JM. 2007. Multilevel interactions between ethylene and auxin in Arabidopsis roots. The Plant Cell 19: 2169-2185
155. Sugimoto Y, Ali AM, Yabuta S, Kinoshita H, Inanaga S, Itai A. 2003. Germination strategy of Striga hermonthica involves regulation of ethylene biosynthesis. Physiologia Plantarum 119: 137-145
156. Sukumar P, Legué V, Vayssières A, et al. 2013. Involvement of auxin pathways in modulating root architecture during beneficial plant-microorganism interactions. Plant, Cell and Environment 36: 909-919
157. Sun J, Xu Y, Ye S, et al. 2009. Arabidopsis ASA1 is important for jasmonatemediated regulation of auxin biosynthesis and transport during lateral root formation. The Plant Cell 21: 1495-1511
158. Sun J, Chen Q, Qi L, et al. 2011. Jasmonate modulates endocytosis and plasma membrane accumulation of the Arabidopsis PIN2 protein. New Phytologist 191: 360-375
159. Thibaud MC, Arrighi JF, Bayle V, et al. 2010. Dissection of local and systemic transcriptional responses to phosphate starvation in Arabidopsis. The Plant Journal 64: 775-789
160. Ticconi CA, Lucero RD, Sakhonwasee S, et al. 2009. ER-resident proteins PDR2 and LPR1 mediate the developmental response of root meristems to phosphate availability. Proceedings of the National Academy of Sciences, USA 106: 14174-14179
161. Tisserant B, Schellenbaum L, Gianinazzi-Pearson V, Gianinazzi S, Berta G. 1992. Influence of infection by an endomycorrhizal fungus on root development and architecture in Platanus acerifolia. Allionia 30: 171-181
162. Tisserant B, Gianinazzi S, Gianinazzi-Pearson V. 1996. Relationships between lateral root order, arbuscular mycorrhiza development, and the physiological state of the symbiotic fungus in Platanus acerifolia. Canadian Journal of Botany 74: 1947-1955
163. Torelli A, Trotta A, Acerbi L, Arcidiacono G, Berta G, Branca C. 2000. IAA and ZR content in leek (Allium porrum L) as influenced by P nutrition and arbuscular mycorrhizae, in relation to plant development. Plant and Soil 226: 29-35
164. Trotta A, Carminati C, Schellenbaum L, Scannerini S, Fusconi, Berta G. 1991. Correlation between root morphogenesis, VA mycorrhizal infection and phosphorus nutrition. In: McMichael BL, Person H, eds. Plant roots and their environment. Amsterdam: Elsevier, 333-339
165. Vance CP, Uhde-Stone C, Allan DL.2003. Phosphorus acquisition and use: Critical adaptation by plants for securing a non-renewable resource. New Phytologist 157: 423-447
166. Van Rhijn P, Fang Y, Galili S, et al. 1997. Expression of early nodulin genes in alfalfa mycorrhizae indicates that signal transduction pathways used in forming arbuscular mycorrhizae and Rhizobium-induced nodules may be conserved. Proceedings of the National Academy of Sciences, USA 94: 5467-5472
167. Vanstraelen M, Benková E. 2012. Hormonal interactions in the regulation of plant development. Annual Review of Cell and Developmental Biology 28: 463-487
168. Volpe V, Delĺaglio E, Giovanetti M, et al. 2012. An AM-induced, MYB-family gene of Lotus japonicus (LjMAMI) affects root growth in an AM-independent manner. The Plant Journal 73: 442-455
169. Volpe V, Delĺaglio E, Bonfante P. 2013. The Lotus japonicusMAMIgene links root development, arbuscular mycorrhizal symbiosis and phosphate availability. Plant Signaling and Behavior 8: E23414
170. Waters MT, Brewer PB, Bussell JD, Smith SM, Beveridge CA. 2012. The Arabidopsis ortholog of rice DWARF27 acts upstream of MAX1 in the control of plant development by strigolactones. Plant Physiology 159: 1073-1085
171. Westwood JH. 2000. Characterization of the Orobanche-Arabidopsis system for studying parasite-host interactions. Weed Science 48: 742-748
172. Werner T, Nehnevajova E, Köllmer I, et al. 2010. Root-specific reduction of cytokinin causes enhanced root growth, drought tolerance, and leaf mineral enrichment in Arabidopsis and tobacco. The Plant Cell 22: 3905-3920
173. Wiersum LK. 1958. Density of root branching as affected by substrate and separate ions. Acta Botanica Neerlandica 7: 174-190
174. Williamson LC, Ribrioux SPCP, Fitter AH, Leyser HMO. 2001. Phosphate availability regulates root system architecture in Arabidopsis. Plant Physiology 126: 875-882
175. Yoneyama K, Xie X, Kim HI, et al. 2012. How do nitrogen and phosphorus deficiencies affect strigolactone production and exudatioñ Planta 235: 1197-1207
176. Yoshida S, Kameoka H, Tempo M, et al. 2012. The D3 F-box protein is a key component in host strigolactone responses essential for arbuscular mycorrhizal symbiosis. New Phytologist 196: 1208-1216
177. Zhou J, Jiao FC, Wu Z, et al. 2008.OsPHR2is involved in phosphate-starvation signaling and excessive phosphate accumulation in shoots of plants. Plant Physiology 146: 1673-1686
178. Zhou K, Yamagishi M, Mitsuru Osaki M, Masuda K. 2008. Sugar signalling mediates cluster root formation and phosphorus starvation-induced gene expression in white lupin. Journal of Experimental Botany 59: 2749-2756