Integrative phenotyping analyses reveal the relevance of the phyB-PIF4 pathway in Arabidopsis thaliana reproductive organs at high ambient temperature
Jazyk angličtina Země Anglie, Velká Británie Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
CZ.02.1.01/0.0/0.0/16_026/0008446
Ministerstvo Školství, Mládeže a Tělovýchovy
CZ.02.1.01/0.0/0.0/16_026/0008446
Ministerstvo Školství, Mládeže a Tělovýchovy
CZ.02.1.01/0.0/0.0/16_026/0008446
Ministerstvo Školství, Mládeže a Tělovýchovy
CZ.02.1.01/0.0/0.0/16_026/0008446
Ministerstvo Školství, Mládeže a Tělovýchovy
CZ.02.1.01/0.0/0.0/16_026/0008446
Ministerstvo Školství, Mládeže a Tělovýchovy
PubMed
39075366
PubMed Central
PMC11285529
DOI
10.1186/s12870-024-05394-w
PII: 10.1186/s12870-024-05394-w
Knihovny.cz E-zdroje
- Klíčová slova
- Arabidopsis, Automatic phenotyping, PIF4, Pistils, Pollen tube guidance, Seeds, Thermomorphogenesis, phyB,
- MeSH
- Arabidopsis * genetika metabolismus růst a vývoj fyziologie MeSH
- fenotyp * MeSH
- fytochrom B * metabolismus genetika MeSH
- kořeny rostlin genetika metabolismus růst a vývoj MeSH
- květy genetika růst a vývoj MeSH
- proteiny huseníčku * genetika metabolismus MeSH
- regulace genové exprese u rostlin MeSH
- signální transdukce MeSH
- transkripční faktory bHLH * genetika metabolismus MeSH
- vysoká teplota MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- fytochrom B * MeSH
- PHYB protein, Arabidopsis MeSH Prohlížeč
- PIF4 protein, Arabidopsis MeSH Prohlížeč
- proteiny huseníčku * MeSH
- transkripční faktory bHLH * MeSH
BACKGROUND: The increasing ambient temperature significantly impacts plant growth, development, and reproduction. Uncovering the temperature-regulating mechanisms in plants is of high importance, for increasing our fundamental understanding of plant thermomorphogenesis, for its potential in applied science, and for aiding plant breeders in improving plant thermoresilience. Thermomorphogenesis, the developmental response to warm temperatures, has been primarily studied in seedlings and in the regulation of flowering time. PHYTOCHROME B and PHYTOCHROME-INTERACTING FACTORs (PIFs), particularly PIF4, are key components of this response. However, the thermoresponse of other adult vegetative tissues and reproductive structures has not been systematically evaluated, especially concerning the involvement of phyB and PIFs. RESULTS: We screened the temperature responses of the wild type and several phyB-PIF4 pathway Arabidopsis mutant lines in combined and integrative phenotyping platforms for root growth in soil, shoot, inflorescence, and seed. Our findings demonstrate that phyB-PIF4 is generally involved in the relay of temperature signals throughout plant development, including the reproductive stage. Furthermore, we identified correlative responses to high ambient temperature between shoot and root tissues. This integrative and automated phenotyping was complemented by monitoring the changes in transcript levels in reproductive organs. Transcriptomic profiling of the pistils from plants grown under high ambient temperature identified key elements that may provide insight into the molecular mechanisms behind temperature-induced reduced fertilization rate. These include a downregulation of auxin metabolism, upregulation of genes involved auxin signalling, miRNA156 and miRNA160 pathways, and pollen tube attractants. CONCLUSIONS: Our findings demonstrate that phyB-PIF4 involvement in the interpretation of temperature signals is pervasive throughout plant development, including processes directly linked to reproduction.
Zobrazit více v PubMed
Wolkovich EM, Cook BI, Allen JM, Crimmins TM, Betancourt JL, Travers SE, et al. Warming experiments underpredict plant phenological responses to climate change. Nature. 2012;485:494–7. 10.1038/nature11014 PubMed DOI
Legris M, Nieto C, Sellaro R, Prat S, Casal JJ. Perception and signalling of light and temperature cues in plants. Plant J. 2017;90:683–97. 10.1111/tpj.13467 PubMed DOI
Sánchez B, Rasmussen A, Porter JR. Temperatures and the growth and development of maize and rice: a review. Glob Chang Biol. 2014;20:408–17. 10.1111/gcb.12389 PubMed DOI
Luo Q. Temperature thresholds and crop production: a review. Clim Change. 2011;109:583–98.10.1007/s10584-011-0028-6 DOI
Ohama N, Sato H, Shinozaki K, Yamaguchi-Shinozaki K. Transcriptional Regulatory Network of Plant Heat Stress Response. Trends Plant Sci. 2017;22:53–65. 10.1016/j.tplants.2016.08.015 PubMed DOI
Hayes S, Schachtschabel J, Mishkind M, Munnik T, Arisz SA. Hot topic: Thermosensing in plants. Plant Cell Environ. 2021;44:2018–33. 10.1111/pce.13979 PubMed DOI PMC
Patel D, Franklin KA. Temperature-regulation of plant architecture. Plant Signal Behav. 2009;4:577–9. 10.4161/psb.4.7.8849 PubMed DOI PMC
Nozue K, Harmer SL, Maloof JN. Genomic analysis of circadian Clock-, Light-, and growth-correlated genes reveals PHYTOCHROME-INTERACTING FACTOR5 as a modulator of Auxin Signaling in Arabidopsis. Plant Physiol. 2011;156:357–72. 10.1104/pp.111.172684 PubMed DOI PMC
Franklin KA, Lee SH, Patel D, Kumar SV, Spartz AK, Gu C, et al. PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) regulates auxin biosynthesis at high temperature. PNAS. 2011;108:20231–5. 10.1073/pnas.1110682108 PubMed DOI PMC
Li B, Jiang S, Gao L, Wang W, Luo H, Dong Y, et al. Heat shock factor A1s are required for phytochrome-interacting factor 4‐Mediated thermomorphogenesis in Arabidopsis. J Integr Plant Biol. 2023. 10.1111/jipb.13579. 10.1111/jipb.13579 PubMed DOI
Nozue K, Covington MF, Duek PD, Lorrain S, Fankhauser C, Harmer SL, et al. Rhythmic growth explained by coincidence between internal and external cues. Nature. 2007;448:358–61. 10.1038/nature05946 PubMed DOI
Legris M, Klose C, Burgie ES, Rojas CCR, Neme M, Hiltbrunner A, et al. Phytochrome B integrates light and temperature signals in Arabidopsis. Science. 2016;354:897–900. 10.1126/science.aaf5656 PubMed DOI
Koini MA, Alvey L, Allen T, Tilley CA, Harberd NP, Whitelam GC, et al. High temperature-mediated adaptations in Plant Architecture require the bHLH transcription factor PIF4. Curr Biol. 2009;19:408–13. 10.1016/j.cub.2009.01.046 PubMed DOI
Trupkin SA, Legris M, Buchovsky AS, Rivero MBT, Casal JJ, Phytochrome B. Nuclear bodies Respond to the low red to far-red ratio and to the reduced irradiance of Canopy Shade in Arabidopsis. Plant Physiol. 2014;165:1698–708. 10.1104/pp.114.242438 PubMed DOI PMC
Galvão RM, Li M, Kothadia SM, Haskel JD, Decker PV, Buskirk EKV, et al. Photoactivated phytochromes interact with HEMERA and promote its accumulation to establish photomorphogenesis in Arabidopsis. Genes Dev. 2012;26:1851–63. 10.1101/gad.193219.112 PubMed DOI PMC
Lorrain S, Allen T, Duek PD, Whitelam GC, Fankhauser C. Phytochrome-mediated inhibition of shade avoidance involves degradation of growth-promoting bHLH transcription factors. Plant J. 2007;53:312–23. 10.1111/j.1365-313X.2007.03341.x PubMed DOI
Huq E, Quail PH. PIF4, a phytochrome-interacting bHLH factor, functions as a negative regulator of phytochrome B signaling in Arabidopsis. EMBO J. 2002;21:2441–50. 10.1093/emboj/21.10.2441 PubMed DOI PMC
Jung J-H, Domijan M, Klose C, Biswas S, Ezer D, Gao M, et al. Phytochromes function as thermosensors in Arabidopsis. Science. 2016;354:886–9. 10.1126/science.aaf6005 PubMed DOI
Casal JJ, Balasubramanian S, Thermomorphogenesis. Annu Rev Plant Biol. 2019;70:1–26. 10.1146/annurev-arplant-050718-095919 PubMed DOI
Sun J, Qi L, Li Y, Chu J, Li C. PIF4-Mediated activation of YUCCA8 expression integrates temperature into the Auxin Pathway in regulating Arabidopsis Hypocotyl Growth. PLoS Genet. 2012;8:e1002594–1002594. 10.1371/journal.pgen.1002594 PubMed DOI PMC
Gray WM, Ostin A, Sandberg G, Romano CP, Estelle M. High temperature promotes auxin-mediated hypocotyl elongation in Arabidopsis. PNAS. 1998;95:7197–202. 10.1073/pnas.95.12.7197 PubMed DOI PMC
Kumar SV, Lucyshyn D, Jaeger KE, Alós E, Alvey E, Harberd NP, et al. PHYTOCHROME INTERACTING FACTOR4 controls the thermosensory activation of flowering. Nature. 2012;484:242–5. 10.1038/nature10928 PubMed DOI PMC
Resentini F, Orozco-Arroyo G, Cucinotta M, Mendes MA. The impact of heat stress in plant reproduction. Front Plant Sci. 2023;14:1271644. 10.3389/fpls.2023.1271644 PubMed DOI PMC
Jiang Y, Lahlali R, Karunakaran C, Warkentin TD, Davis AR, Bueckert RA. Pollen, ovules and pollination in pea: success, failure and resilience in heat. Plant Cell Environ. 2019;42:354–72. 10.1111/pce.13427 PubMed DOI
Das S, Krishnan P, Nayak M, Ramakrishnan B. High temperature stress effects on pollens of rice (Oryza sativa L.) genotypes. Environ Exp Bot. 2014;101:36–46.10.1016/j.envexpbot.2014.01.004 DOI
Devasirvatham V, Gaur PM, Mallikarjuna N, Raju TN, Trethowan RM, Tan DKY. Reproductive biology of chickpea response to heat stress in the field is associated with the performance in controlled environments. Field Crops Res. 2013;142:9–19.10.1016/j.fcr.2012.11.011 DOI
Talukder ASMHM, McDonald GK, Gill GS. Effect of short-term heat stress prior to flowering and early grain set on the grain yield of wheat. Field Crops Res. 2014;160:54–63.10.1016/j.fcr.2014.01.013 DOI
Lin C-J, Li C-Y, Lin S-K, Yang F-H, Huang J-J, Liu Y-H, et al. Influence of high temperature during grain filling on the accumulation of storage proteins and grain quality in rice (Oryza sativa L). J Agric Food Chem. 2010;58:10545–52. 10.1021/jf101575j PubMed DOI
Jumrani K, Bhatia VS. Impact of elevated temperatures on growth and yield of chickpea (Cicer arietinum L). Field Crops Res. 2014;164:90–7.10.1016/j.fcr.2014.06.003 DOI
Mácová K, Prabhullachandran U, Štefková M, Spyroglou I, Pěnčík A, Endlová L, et al. Long-term high-temperature stress impacts on embryo and seed development in Brassica napus. Front Plant Sci. 2022;13:844292. 10.3389/fpls.2022.844292 PubMed DOI PMC
Elferjani R, Soolanayakanahally R. Canola responses to Drought, Heat, and combined stress: Shared and Specific effects on Carbon Assimilation, seed yield, and oil composition. Front Plant Sci. 2018;9:1224. 10.3389/fpls.2018.01224 PubMed DOI PMC
Jedličková V, Hejret V, Demko M, Jedlička P, Štefková M, Robert HS. Transcriptome analysis of thermomorphogenesis in ovules and during early seed development in Brassica napus. BMC Genomics. 2023;24:236. 10.1186/s12864-023-09316-2 PubMed DOI PMC
Canales J, Verdejo JF, Calderini DF. Transcriptome and physiological analysis of Rapeseed Tolerance to Post-flowering temperature increase. Int J Mol Sci. 2023;24:15593. 10.3390/ijms242115593 PubMed DOI PMC
Scholl RL, May ST, Ware DH. Seed and Molecular resources for Arabidopsis. Plant Physiol. 2000;124:1477–80. 10.1104/pp.124.4.1477 PubMed DOI PMC
Leivar P, Monte E, Al-Sady B, Carle C, Storer A, Alonso JM, et al. The Arabidopsis phytochrome-interacting factor PIF7, together with PIF3 and PIF4, regulates responses to prolonged red light by modulating phyB levels. Plant cell. 2008;20:337–52. 10.1105/tpc.107.052142 PubMed DOI PMC
Oh S, Warnasooriya SN, Montgomery BL. Downstream effectors of light- and phytochrome-dependent regulation of hypocotyl elongation in Arabidopsis thaliana. Plant Mol Biol. 2013;81:627–40. 10.1007/s11103-013-0029-0 PubMed DOI PMC
Robert HS, Grones P, Stepanova AN, Robles LM, Lokerse AS, Alonso JM, et al. Local Auxin sources Orient the apical-basal Axis in Arabidopsis embryos. Curr Biol. 2013;23:2506–12. 10.1016/j.cub.2013.09.039 PubMed DOI
Stepanova AN, Robertson-Hoyt J, Yun JJ, Benavente LM, Xie D-Y, Dolezal K, et al. TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell. 2008;133:177–91. 10.1016/j.cell.2008.01.047 PubMed DOI
Oh E, Zhu J-Y, Wang Z-Y. Interaction between BZR1 and PIF4 integrates brassinosteroid and environmental responses. Nat Cell Biol. 2012;14:802–9. 10.1038/ncb2545 PubMed DOI PMC
Šmeringai J, Rudolf J, Trtílek M, Schrumpfová PP, Pernisová M. Shoot phenotyping of cytokinin receptors mutants revealed fluorescence parameters as early markers of drought stress. bioRxiv. 2023. 2023.11.30.569457.
Awlia M, Nigro A, Fajkus J, Schmoeckel SM, Negrão S, Santelia D, et al. High-throughput non-destructive phenotyping of traits that contribute to Salinity Tolerance in Arabidopsis thaliana. Front Plant Sci. 2016;7:1414. 10.3389/fpls.2016.01414 PubMed DOI PMC
Alexander MP. Differential staining of aborted and nonaborted pollen. Stain Technol. 1969;44:117–22. 10.3109/10520296909063335 PubMed DOI
Attuluri VPS, López JFS, Maier L, Paruch K, Robert HS. Comparing the efficiency of six clearing methods in developing seeds of Arabidopsis thaliana. Plant Reprod. 2022;35:279–93. 10.1007/s00497-022-00453-4 PubMed DOI PMC
Postma M, Goedhart J. PlotsOfData—A web app for visualizing data together with their summaries. PLoS Biol. 2019;17:e3000202. 10.1371/journal.pbio.3000202 PubMed DOI PMC
Love MI, Huber W, Anders S. Moderated estimation of Fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:550. 10.1186/s13059-014-0550-8 PubMed DOI PMC
Kinsella RJ, Kähäri A, Haider S, Zamora J, Proctor G, Spudich G, et al. Ensembl BioMarts: a hub for data retrieval across taxonomic space. Database. 2011;2011:bar030. 10.1093/database/bar030 PubMed DOI PMC
Wu T, Hu E, Xu S, Chen M, Guo P, Dai Z, et al. clusterProfiler 4.0: a universal enrichment tool for interpreting omics data. Innov. 2021;2:100141. PubMed PMC
Wickham H. ggplot2, Elegant Graphics for Data Analysis. R. 2016. 10.1007/978-3-319-24277-4.
Silva-Navas J, Moreno‐Risueno MA, Manzano C, Pallero‐Baena M, Navarro‐Neila S, Téllez‐Robledo B, et al. D‐Root: a system for cultivating plants with the roots in darkness or under different light conditions. Plant J. 2015;84:244–55. 10.1111/tpj.12998 PubMed DOI
González-García MP, Conesa CM, Lozano-Enguita A, Baca-González V, Simancas B, Navarro-Neila S, et al. Temperature changes in the root ecosystem affect plant functionality. Plant Commun. 2023;4:100514. 10.1016/j.xplc.2022.100514 PubMed DOI PMC
Ong P, Jian J, Li X, Yin J, Ma G. Visible and near-infrared spectroscopic determination of sugarcane chlorophyll content using a modified wavelength selection method for multivariate calibration. Spectrochim Acta Part A. Mol Biomol Spectrosc. 2023;305:123477.10.1016/j.saa.2023.123477 PubMed DOI
Liu L, Zareef M, Wang Z, Li H, Chen Q, Ouyang Q. Monitoring chlorophyll changes during Tencha processing using portable near-infrared spectroscopy. Food Chem. 2023;412:135505. 10.1016/j.foodchem.2023.135505 PubMed DOI
Li C, Li H, Li J, Lei Y, Li C, Manevski K, et al. Using NDVI percentiles to monitor real-time crop growth. Comput Electron Agric. 2019;162:357–63.10.1016/j.compag.2019.04.026 DOI
Payares LKA, Tarquis AM, Peralo RH, Cano J, Cámara J, Nowack J, et al. Multispectral and thermal sensors onboard UAVs for heterogeneity in Merlot Vineyard detection: contribution to Zoning maps. Remote Sens. 2023;15:4024.10.3390/rs15164024 DOI
Peñuelas J, Filella I, Gamon JA. Assessment of photosynthetic radiation-use efficiency with spectral reflectance. N Phytol. 1995;131:291–6.10.1111/j.1469-8137.1995.tb03064.x DOI
Haboudane D, Miller JR, Pattey E, Zarco-Tejada PJ, Strachan IB. Hyperspectral vegetation indices and novel algorithms for predicting green LAI of crop canopies: modeling and validation in the context of precision agriculture. Remote Sens Environ. 2004;90:337–52.10.1016/j.rse.2003.12.013 DOI
Murchie EH, Lawson T. Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications. J Exp Bot. 2013;64:3983–98. 10.1093/jxb/ert208 PubMed DOI
Ruban AV. Evolution under the sun: optimizing light harvesting in photosynthesis. J Exp Bot. 2015;66:7–23. 10.1093/jxb/eru400 PubMed DOI
Yang X, Dong G, Palaniappan K, Mi G, Baskin TI. Temperature-compensated cell production rate and elongation zone length in the root of Arabidopsis thaliana. Plant Cell Environ. 2017;40:264–76. 10.1111/pce.12855 PubMed DOI
Xie Y, Liu Y, Wang H, Ma X, Wang B, Wu G, et al. Phytochrome-interacting factors directly suppress MIR156 expression to enhance shade-avoidance syndrome in Arabidopsis. Nat Commun. 2017;8:348. 10.1038/s41467-017-00404-y PubMed DOI PMC
Sang Q, Fan L, Liu T, Qiu Y, Du J, Mo B, et al. MicroRNA156 conditions auxin sensitivity to enable growth plasticity in response to environmental changes in Arabidopsis. Nat Commun. 2023;14:1449. 10.1038/s41467-023-36774-9 PubMed DOI PMC
Kulkarni SR, Vaneechoutte D, Van de Velde J, Vandepoele K. TF2Network: predicting transcription factor regulators and gene regulatory networks in Arabidopsis using publicly available binding site information. Nucleic Acids Res. 2017;46:gkx1279. PubMed PMC
Takeuchi H, Higashiyama TA, Species-Specific. Cluster of Defensin-Like genes encodes Diffusible Pollen Tube attractants in Arabidopsis. PLoS Biol. 2012;10:e1001449. 10.1371/journal.pbio.1001449 PubMed DOI PMC
Costa LM, Marshall E, Tesfaye M, Silverstein KAT, Mori M, Umetsu Y, et al. Central cell-derived peptides regulate early embryo patterning in flowering plants. Science. 2014;344:168–72. 10.1126/science.1243005 PubMed DOI
Robert HS, Park C, Gutièrrez CL, Wójcikowska B, Pěnčík A, Novák O, et al. Maternal auxin supply contributes to early embryo patterning in Arabidopsis. Nat Plants. 2018;4:548–53. 10.1038/s41477-018-0204-z PubMed DOI PMC
Kumar SV, Lucyshyn D, Jaeger KE, Alós E, Alvey E, Harberd NP, et al. Transcription factor PIF4 controls the thermosensory activation of flowering. Nature. 2012;484:242–5. 10.1038/nature10928 PubMed DOI PMC
Song J, Liu Q, Hu B, Wu W. Photoreceptor PhyB involved in Arabidopsis temperature perception and heat-tolerance formation. Int J Mol Sci. 2017;18:1194. 10.3390/ijms18061194 PubMed DOI PMC
Liu J, Liu Y, Wang S, Cui Y, Yan D. Heat stress reduces Root Meristem size via induction of Plasmodesmal Callose Accumulation Inhibiting Phloem Unloading in Arabidopsis. Int J Mol Sci. 2022;23:2063. 10.3390/ijms23042063 PubMed DOI PMC
Wang R, Zhang Y, Kieffer MM, Yu H, Kepinski S, Estelle M. HSP90 regulates temperature-dependent seedling growth in Arabidopsis by stabilizing the auxin co-receptor F-box protein TIR1. Nat Commun. 2016;7:10269–10269. 10.1038/ncomms10269 PubMed DOI PMC
Parveen S, Rahman A. Actin isovariant ACT7 modulates Root Thermomorphogenesis by altering Intracellular Auxin Homeostasis. Int J Mol Sci. 2021;22:7749. 10.3390/ijms22147749 PubMed DOI PMC
Li Q-Q, Zhang Z, Zhang C-X, Wang Y-L, Liu C-B, Wu J-C, et al. Phytochrome-interacting factors orchestrate hypocotyl adventitious root initiation in Arabidopsis. Development. 2022;149:dev200362. 10.1242/dev.200362 PubMed DOI
Gaillochet C, Burko Y, Platre MP, Zhang L, Simura J, Willige BC, et al. HY5 and phytochrome activity modulate shoot-to-root coordination during thermomorphogenesis in Arabidopsis. Development. 2020;147:dev192625. 10.1242/dev.192625 PubMed DOI PMC
Lee S, Wang W, Huq E. Spatial regulation of thermomorphogenesis by HY5 and PIF4 in Arabidopsis. Nat Commun. 2021;12:3656. 10.1038/s41467-021-24018-7 PubMed DOI PMC
Franklin KA. Light and temperature signal crosstalk in plant development. Curr Opin Plant Biol. 2009;12:63–8. 10.1016/j.pbi.2008.09.007 PubMed DOI
Jagadish SVK, Bahuguna RN, Djanaguiraman M, Gamuyao R, Prasad PVV, Craufurd PQ. Implications of high temperature and elevated CO2 on flowering time in plants. Front Plant Sci. 2016;7:913. 10.3389/fpls.2016.00913 PubMed DOI PMC
Cao Z, Yao X, Liu H, Liu B, Cheng T, Tian Y, et al. Comparison of the abilities of vegetation indices and photosynthetic parameters to detect heat stress in wheat. Agric Meteorol. 2019;265:121–36.10.1016/j.agrformet.2018.11.009 DOI
Barnabás B, Jäger K, Fehér A. The effect of drought and heat stress on reproductive processes in cereals. Plant Cell Environ. 2008;31:11–38. 10.1111/j.1365-3040.2007.01727.x PubMed DOI
Zhang S-S, Yang H, Ding L, Song Z-T, Ma H, Chang F, et al. Tissue-specific Transcriptomics reveals an important role of the unfolded protein response in maintaining fertility upon heat stress in Arabidopsis. Plant Cell. 2017;29:1007–23. 10.1105/tpc.16.00916 PubMed DOI PMC
Lohani N, Singh MB, Bhalla PL. High temperature susceptibility of sexual reproduction in crop plants. J Exp Bot. 2020;71:555–68. 10.1093/jxb/erz426 PubMed DOI
Storme ND, Geelen D. High temperatures alter cross-over distribution and induce male meiotic restitution in Arabidopsis thaliana. Commun Biol. 2020;3:187. 10.1038/s42003-020-0897-1 PubMed DOI PMC
Zhang M, Zhang X, Wang R, Zang R, Guo L, Qi T, et al. Heat-responsive microRNAs participate in regulating the pollen fertility stability of CMS-D2 restorer line under high-temperature stress. Biol Res. 2023;56:58. 10.1186/s40659-023-00465-y PubMed DOI PMC
Wu M-F, Tian Q, Reed JW. Arabidopsis microRNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction. Development. 2006;133:4211–8. 10.1242/dev.02602 PubMed DOI
Oshino T, Miura S, Kikuchi S, Hamada K, Yano K, Watanabe M, et al. Auxin depletion in barley plants under high-temperature conditions represses DNA proliferation in organelles and nuclei via transcriptional alterations. Plant Cell Environ. 2011;34:284–90. 10.1111/j.1365-3040.2010.02242.x PubMed DOI
Sakata T, Oshino T, Miura S, Tomabechi M, Tsunaga Y, Higashitani N, et al. Auxins reverse plant male sterility caused by high temperatures. PNAS. 2010;107:8569–74. 10.1073/pnas.1000869107 PubMed DOI PMC
Higashitani A. High temperature injury and auxin biosynthesis in microsporogenesis. Front Plant Sci. 2013;4:47. 10.3389/fpls.2013.00047 PubMed DOI PMC
Irenaeus T, Mitra SK. Understanding the pollen and ovule characters and fruit set of fruit crops in relation to temperature and genotype – a review. J Appl Bot Food Qual. 2014;87.
Huang Z, Footitt S, Finch-Savage WE. The effect of temperature on reproduction in the summer and winter annual Arabidopsis thaliana ecotypes Bur and Cvi. Ann Bot. 2014;113:921–9. 10.1093/aob/mcu014 PubMed DOI PMC
Whittle CA, Otto SP, Johnston MO, Krochko JE. Adaptive epigenetic memory of ancestral temperature regime in Arabidopsis thalianaThis paper is one of a selection of papers published in a special issue from the National Research Council of Canada Plant Biotechnology Institute. Botany. 2009;87:650–7.10.1139/B09-030 DOI