Transcription Factor IAA27 Positively Regulates P Uptake through Promoted Adventitious Root Development in Apple Plants

Phosphate (P) deficiency severely limits the growth and production of plants. Adventitious root development plays an essential role in responding to low phosphorus stress for apple plants. However, the molecular mechanisms regulating adventitious root growth and development in response to low phosphorus stress have remained elusive. In this study, a mutation (C-T) in the coding region of the apple AUXIN/INDOLE-3-ACETIC ACID 27 (IAA27) gene was identified. MdIAA27T-overexpressing transgenic apple improved the tolerance to phosphorus deficiency, which grew longer and denser adventitious roots and presented higher phosphorous content than the control plants under low phosphorus conditions, while the overexpression of MdIAA27C displayed the opposite trend. Moreover, the heterologous overexpression of MdIAA27 in tobacco yielded the same results, supporting the aforementioned findings. In vitro and in vivo assays showed that MdIAA27 directly interacted with AUXIN RESPONSE FACTOR (ARF8), ARF26 and ARF27, which regulated Small Auxin-Up RNA 76 (MdSAUR76) and lateral organ boundaries domain 16 (MdLBD16) transcription. The mutation in IAA27 resulted in altered interaction modes, which in turn promoted the release of positive ARFs to upregulate SAUR76 and LBD16 expression in low phosphorus conditions. Altogether, our studies provide insights into how the allelic variation of IAA27 affects adventitious root development in response to low phosphorus stress.

[1]  Yong Guo,et al.  GmIAA27 Encodes an AUX/IAA Protein Involved in Dwarfing and Multi-Branching in Soybean , 2022, International journal of molecular sciences.

[2]  Hairong Wei,et al.  Two high hierarchical regulators, PuMYB40 and PuWRKY75, control the low phosphorus driven adventitious root formation in Populus ussuriensis , 2022, Plant biotechnology journal.

[3]  Zhenhai Han,et al.  Ethylene response factor MdERF4 and histone deacetylase MdHDA19 suppress apple fruit ripening through histone deacetylation of ripening-related genes , 2022, Plant physiology.

[4]  OUP accepted manuscript , 2022, Plant Physiology.

[5]  F. Ma,et al.  Overexpression of auxin response gene MdIAA24 enhanced cadmium tolerance in apple (Malus domestica). , 2021, Ecotoxicology and environmental safety.

[6]  Xu Li,et al.  An HD-ZIP transcription factor, MxHB13, integrates auxin-regulated and juvenility-determined control of adventitious rooting in Malus xiaojinensis. , 2021, The Plant journal : for cell and molecular biology.

[7]  Baocun Zhao,et al.  OsIAA20, an Aux/IAA protein, mediates abiotic stress tolerance in rice through an ABA pathway. , 2021, Plant science : an international journal of experimental plant biology.

[8]  Jia Li,et al.  SAUR15 Promotes Lateral and Adventitious Root Development via Activating H+-ATPases and Auxin Biosynthesis. , 2020, Plant physiology.

[9]  C. You,et al.  Apple SUMO E3 ligase MdSIZ1 facilitates SUMOylation of MdARF8 to regulate lateral root formation. , 2020, The New phytologist.

[10]  Guodong Yang,et al.  Function identification of MdTIR1 in apple root growth benefited from the predicted MdPPI network , 2020 .

[11]  Rui Li,et al.  Overexpression of MdPHR1 Enhanced Tolerance to Phosphorus Deficiency by Increasing MdPAP10 Transcription in Apple (Malus ×  Domestica) , 2020 .

[12]  Jia Li,et al.  SAUR15 Promotes Lateral and Adventitious Root Development via Activating H+-ATPases and Auxin Biosynthesis1 , 2020, Plant Physiology.

[13]  W. Liao,et al.  The role and proteomic analysis of ethylene in hydrogen gas-induced adventitious rooting development in cucumber (Cucumis sativus L.) explants , 2020, PeerJ.

[14]  Xiaoqing Yang,et al.  The bZIP53–IAA4 module inhibits adventitious root development in Populus , 2020, Journal of experimental botany.

[15]  Zhenhai Han,et al.  Ethylene Response Factors MbERF4 and MbERF72 Suppress Iron Uptake in Woody Apple Plants by Modulating Rhizosphere pH. , 2019, Plant & cell physiology.

[16]  T. Darch,et al.  Phosphorus use efficiency and fertilizers: future opportunities for improvements , 2019, Frontiers of Agricultural Science and Engineering.

[17]  C. You,et al.  Functional identification of apple MdMYB2 gene in phosphate-starvation response. , 2019, Journal of plant physiology.

[18]  S. van Nocker,et al.  Overexpression of MdIAA9 confers high tolerance to osmotic stress in transgenic tobacco , 2019, PeerJ.

[19]  J. Ecker,et al.  Auxin-sensitive Aux/IAA proteins mediate drought tolerance in Arabidopsis by regulating glucosinolate levels , 2019, Nature Communications.

[20]  N. Thiffault,et al.  Root system origin and structure influence planting shock of black spruce seedlings in boreal microsites , 2019, Forest Ecology and Management.

[21]  Shashank K. Pandey,et al.  LBD16 and LBD18 acting downstream of ARF7 and ARF19 are involved in adventitious root formation in Arabidopsis , 2019, BMC Plant Biology.

[22]  Y. Hao,et al.  The SUMO E3 Ligase MdSIZ1 Targets MdbHLH104 to Regulate Plasma Membrane H+-ATPase Activity and Iron Homeostasis1[OPEN] , 2018, Plant Physiology.

[23]  Haiying Yu,et al.  Quantitative trait locus analysis of adventitious and lateral root morphology of barley grown at low and high P. , 2018, Functional plant biology : FPB.

[24]  Peng Qin,et al.  Pivotal role of LBD16 in root and root-like organ initiation , 2018, Cellular and Molecular Life Sciences.

[25]  R. Otto,et al.  Nutrient uptake by high-yielding cotton crop in Brazil. , 2018 .

[26]  Zhenhai Han,et al.  An ethylene response factor (MxERF4) functions as a repressor of Fe acquisition in Malus xiaojinensis , 2018, Scientific Reports.

[27]  Zhenhai Han,et al.  MdPIN1b encodes a putative auxin efflux carrier and has different expression patterns in BC and M9 apple rootstocks , 2018, Plant Molecular Biology.

[28]  Z. Qiu,et al.  Physiological and transcriptome analysis of He-Ne laser pretreated wheat seedlings in response to drought stress , 2017, Scientific Reports.

[29]  Xu Li,et al.  High miR156 Expression Is Required for Auxin-Induced Adventitious Root Formation via MxSPL26 Independent of PINs and ARFs in Malus xiaojinensis , 2017, Front. Plant Sci..

[30]  Colleen J. Doherty,et al.  Plant Stress Tolerance Requires Auxin-Sensitive Aux/IAA Transcriptional Repressors , 2017, Current Biology.

[31]  Kai Zhou,et al.  A genome-wide analysis of the ASYMMETRIC LEAVES2/LATERAL ORGAN BOUNDARIES (AS2/LOB) gene family in barley (Hordeum vulgare L.) , 2016, Journal of Zhejiang University-SCIENCE B.

[32]  Ajay Jain,et al.  Deciphering Phosphate Deficiency-Mediated Temporal Effects on Different Root Traits in Rice Grown in a Modified Hydroponic System , 2016, Frontiers in Plant Science.

[33]  W. Gray,et al.  SAUR Proteins as Effectors of Hormonal and Environmental Signals in Plant Growth. , 2015, Molecular plant.

[34]  Jukon Kim,et al.  OsIAA6, a member of the rice Aux/IAA gene family, is involved in drought tolerance and tiller outgrowth. , 2015, Plant science : an international journal of experimental plant biology.

[35]  F. Hochholdinger,et al.  LATERAL ROOT PRIMORDIA 1 of maize acts as a transcriptional activator in auxin signalling downstream of the Aux/IAA gene rootless with undetectable meristem 1 , 2015, Journal of experimental botany.

[36]  Philip N Benfey,et al.  Regulation of plant root system architecture: implications for crop advancement. , 2015, Current opinion in biotechnology.

[37]  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.

[38]  L. Willmitzer,et al.  The transcription factor PHR1 regulates lipid remodeling and triacylglycerol accumulation in Arabidopsis thaliana during phosphorus starvation , 2015, Journal of experimental botany.

[39]  N. von Wirén,et al.  It's time to make changes: modulation of root system architecture by nutrient signals. , 2014, Journal of experimental botany.

[40]  D. Timlin,et al.  Growth, nutrient dynamics, and efficiency responses to carbon dioxide and phosphorus nutrition in soybean , 2014 .

[41]  Iain M Young,et al.  Root hairs improve root penetration, root-soil contact, and phosphorus acquisition in soils of different strength. , 2013, Journal of experimental botany.

[42]  Zeng-Fu Xu,et al.  Ectopic Overexpression of an AUXIN/INDOLE-3-ACETIC ACID (Aux/IAA) Gene OsIAA4 in Rice Induces Morphological Changes and Reduces Responsiveness to Auxin , 2013, International journal of molecular sciences.

[43]  H. Kaminaka,et al.  IAA8 Involved in Lateral Root Formation Interacts with the TIR1 Auxin Receptor and ARF Transcription Factors in Arabidopsis , 2012, PloS one.

[44]  Yutaka Sato,et al.  OsIAA13-mediated auxin signaling is involved in lateral root initiation in rice. , 2012, Plant science : an international journal of experimental plant biology.

[45]  Mondher Bouzayen,et al.  The tomato SlIAA15 is involved in trichome formation and axillary shoot development. , 2012, The New phytologist.

[46]  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.

[47]  Lei Xu,et al.  OsGLU3, a putative membrane-bound endo-1,4-beta-glucanase, is required for root cell elongation and division in rice (Oryza sativa L.). , 2012, Molecular plant.

[48]  L. Nussaume,et al.  Root developmental adaptation to phosphate starvation: better safe than sorry. , 2011, Trends in plant science.

[49]  W. Plaxton,et al.  Metabolic Adaptations of Phosphate-Starved Plants1 , 2011, Plant Physiology.

[50]  Wei-Hua Wu,et al.  The WRKY6 Transcription Factor Modulates PHOSPHATE1 Expression in Response to Low Pi Stress in Arabidopsis[W][OA] , 2009, The Plant Cell Online.

[51]  J. Schwambach,et al.  Phenotypic Plasticity of Adventitious Rooting in Arabidopsis Is Controlled by Complex Regulation of AUXIN RESPONSE FACTOR Transcripts and MicroRNA Abundance[W] , 2009, The Plant Cell Online.

[52]  Jin-Young Park,et al.  Overexpression of IAA1 with domain II mutation impairs cell elongation and cell division in inflorescences and leaves of Arabidopsis. , 2009, Journal of plant physiology.

[53]  L. An,et al.  Hydrogen peroxide acts as a signal molecule in the adventitious root formation of mung bean seedlings , 2009 .

[54]  J. Lynch,et al.  Ethylene insensitivity impedes a subset of responses to phosphorus deficiency in tomato and petunia. , 2008, Plant, cell & environment.

[55]  Keithanne Mockaitis,et al.  Auxin receptors and plant development: a new signaling paradigm. , 2008, Annual review of cell and developmental biology.

[56]  L. Herrera-Estrella,et al.  Transcript profiling of Zea mays roots reveals gene responses to phosphate deficiency at the plant- and species-specific levels. , 2008, Journal of experimental botany.

[57]  Karen S. Osmont,et al.  Hidden branches: developments in root system architecture. , 2007, Annual review of plant biology.

[58]  Ping Wu,et al.  A PIN1 family gene, OsPIN1, involved in auxin-dependent adventitious root emergence and tillering in rice. , 2005, Plant & cell physiology.

[59]  Pierre Frasse,et al.  The Tomato Aux/IAA Transcription Factor IAA9 Is Involved in Fruit Development and Leaf Morphogenesisw⃞ , 2005, The Plant Cell Online.

[60]  K. Ljung,et al.  Auxin and Light Control of Adventitious Rooting in Arabidopsis Require ARGONAUTE1w⃞ , 2005, The Plant Cell Online.

[61]  A. Murphy,et al.  Auxin transport. , 2005, Current opinion in plant biology.

[62]  M. Ryan,et al.  Grain mineral concentrations and yield of wheat grown under organic and conventional management , 2004 .

[63]  E. Liscum,et al.  MASSUGU2 Encodes Aux/IAA19, an Auxin-Regulated Protein That Functions Together with the Transcriptional Activator NPH4/ARF7 to Regulate Differential Growth Responses of Hypocotyl and Formation of Lateral Roots in Arabidopsis thaliana , 2004, The Plant Cell Online.

[64]  A. Karthikeyan,et al.  Phosphate Acquisition , 2004, Plant and Soil.

[65]  L. Herrera-Estrella,et al.  The role of nutrient availability in regulating root architecture. , 2003, Current opinion in plant biology.

[66]  L. Hai.  Effect of Phosphorus Deficiency Stress on Rice Lateral Root Growth and Nutrient Absorption , 2001 .

[67]  S. Abel,et al.  Aux/IAA proteins are phosphorylated by phytochrome in vitro. , 2000, Plant physiology.

[68]  A. Theologis,et al.  Degradation of Aux/IAA proteins is essential for normal auxin signalling. , 2000, The Plant journal : for cell and molecular biology.

[69]  J. Fry,et al.  A simple and general method for transferring genes into plants. , 1985, Science.