Ethylene inhibits rice root elongation in compacted soil via ABA- and auxin-mediated mechanisms

. 2022 Jul 26 ; 119 (30) : e2201072119. [epub] 20220718

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem, Research Support, U.S. Gov't, Non-P.H.S.

Perzistentní odkaz   https://www.medvik.cz/link/pmid35858424

Grantová podpora
BB/V00557X/1 Biotechnology and Biological Sciences Research Council - United Kingdom
BB/T001437/1 Biotechnology and Biological Sciences Research Council - United Kingdom
BB/W008874/1 Biotechnology and Biological Sciences Research Council - United Kingdom
BB/V018124/1 Biotechnology and Biological Sciences Research Council - United Kingdom
BB/S011102/1 Biotechnology and Biological Sciences Research Council - United Kingdom

Soil compaction represents a major agronomic challenge, inhibiting root elongation and impacting crop yields. Roots use ethylene to sense soil compaction as the restricted air space causes this gaseous signal to accumulate around root tips. Ethylene inhibits root elongation and promotes radial expansion in compacted soil, but its mechanistic basis remains unclear. Here, we report that ethylene promotes abscisic acid (ABA) biosynthesis and cortical cell radial expansion. Rice mutants of ABA biosynthetic genes had attenuated cortical cell radial expansion in compacted soil, leading to better penetration. Soil compaction-induced ethylene also up-regulates the auxin biosynthesis gene OsYUC8. Mutants lacking OsYUC8 are better able to penetrate compacted soil. The auxin influx transporter OsAUX1 is also required to mobilize auxin from the root tip to the elongation zone during a root compaction response. Moreover, osaux1 mutants penetrate compacted soil better than the wild-type roots and do not exhibit cortical cell radial expansion. We conclude that ethylene uses auxin and ABA as downstream signals to modify rice root cell elongation and radial expansion, causing root tips to swell and reducing their ability to penetrate compacted soil.

Zobrazit více v PubMed

Hamza M. A., Anderson W. K., Soil compaction in cropping systems: A review of the nature, causes and possible solutions. Soil Tillage Res. 82, 121–145 (2005).

Gregory A. S., et al. , Physical resilience of soil to field compaction and the interactions with plant growth and microbial community structure. Eur. J. Soil Sci. 58, 1221–1232 (2007).

Arvidsson J., Nutrient uptake and growth of barley as affected by soil compaction. Plant Soil 208, 9–19 (1999).

Hoque M., Kobata T., Effect of Soil compaction on the grain yield of rice (Oryza sativa L.) under water-deficit stress during the reproductive stage. Plant Prod. Sci. 3, 316–322 (2000).

Soane B. D., van Ouwerkerk C., Implications of soil compaction in crop production for the quality of the environment. Soil Tillage Res. 35, 5–22 (1995).

Jones A., et al. , The State of Soil in Europe – a Contribution of the JRC to European Environment Agency's Environment State and Outlook Report - SOER 2010. European Commission – EUR 25186 EN – Joint Research Center, 10.2788/77361 (2012). DOI

Schneider H. M., et al. , Multiseriate cortical sclerenchyma enhance root penetration in compacted soils. Proc. Natl. Acad. Sci. U.S.A. 118, e2012087118 (2021). PubMed PMC

Correa J., Postma J. A., Watt M., Wojciechowski T., Soil compaction and the architectural plasticity of root systems. J. Exp. Bot. 70, 6019–6034 (2019). PubMed PMC

Passioura J. B., Soil conditions and plant growth. Plant Cell Environ. 25, 311–318 (2002). PubMed

Pandey B. K., et al. , Plant roots sense soil compaction through restricted ethylene diffusion. Science 371, 276–280 (2021). PubMed

Růzicka K., et al. , Ethylene regulates root growth through effects on auxin biosynthesis and transport-dependent auxin distribution. Plant Cell 19, 2197–2212 (2007). PubMed PMC

Qin H., Huang R., Auxin controlled by ethylene steers root development. Int. J. Mol. Sci. 19, 3656 (2018). PubMed PMC

Swarup R., et al. , Ethylene upregulates auxin biosynthesis in Arabidopsis seedlings to enhance inhibition of root cell elongation. Plant Cell 19, 2186–2196 (2007). PubMed PMC

Jacobsen A. G. R., Jervis G., Xu J., Topping J. F., Lindsey K., Root growth responses to mechanical impedance are regulated by a network of ROS, ethylene and auxin signalling in Arabidopsis. New Phytol. 231, 225–242 (2021). PubMed PMC

Li X., Chen L., Forde B. G., Davies W. J., The biphasic root growth response to abscisic acid in Arabidopsis involves interaction with ethylene and auxin signalling pathways. Front. Plant Sci. 8, 1493 (2017). PubMed PMC

Miao R., et al. , Low ABA concentration promotes root growth and hydrotropism through relief of ABA INSENSITIVE 1-mediated inhibition of plasma membrane H+-ATPase 2. Sci. Adv. 7, 12 (2021). PubMed PMC

Mulholland B. J., et al. , Effect of soil compaction on barley (Hordeum vulgare L.) growth: I. Possible role for ABA as a root-sourced chemical signal. J. Exp. Bot. 47, 539–549 (1996).

Barrero J. M., et al. , Both abscisic acid (ABA)-dependent and ABA-independent pathways govern the induction of NCED3, AAO3 and ABA1 in response to salt stress. Plant Cell Environ. 29, 2000–2008 (2006). PubMed

Ma B., et al. , Identification of rice ethylene-response mutants and characterization of MHZ7/OsEIN2 in distinct ethylene response and yield trait regulation. Mol. Plant 6, 1830–1848 (2013). PubMed

Yin C. C., et al. , Ethylene responses in rice roots and coleoptiles are differentially regulated by a carotenoid isomerase-mediated abscisic acid pathway. Plant Cell 27, 1061–1081 (2015). PubMed PMC

Pandey B. K., Atkinson J. A., Sturrock C. J., Non-invasive imaging of rice roots in non-compacted and compacted soil. Bio Protoc. 11, e4252 (2021). PubMed PMC

Agrawal G. K., et al. , Screening of the rice viviparous mutants generated by endogenous retrotransposon Tos17 insertion. Tagging of a zeaxanthin epoxidase gene and a novel ostatc gene. Plant Physiol. 125, 1248–1257 (2001). PubMed PMC

Liao Y., et al. , Mutation in rice Abscisic Acid2 results in cell death, enhanced disease-resistance, altered seed dormancy and development. Front. Plant Sci. 9, 405 (2018). PubMed PMC

Ma B., et al. , Ethylene-induced inhibition of root growth requires abscisic acid function in rice (Oryza sativa L.) seedlings. PLoS Genet. 10, e1004701 (2014). PubMed PMC

North H. M., et al. , The Arabidopsis ABA-deficient mutant aba4 demonstrates that the major route for stress-induced ABA accumulation is via neoxanthin isomers. Plant J. 50, 810–824 (2007). PubMed

Stepanova A. N., Yun J., Likhacheva A. V., Alonso J. M., Multilevel interactions between ethylene and auxin in Arabidopsis roots. Plant Cell 19, 2169–2185 (2007). PubMed PMC

Yang J., et al. , Dynamic regulation of auxin response during rice development revealed by newly established hormone biosensor markers. Front. Plant Sci. 8, 256 (2017). PubMed PMC

Huang G., et al. , Rice actin binding protein RMD controls crown root angle in response to external phosphate. Nat. Commun. 9, 2346 (2018). PubMed PMC

Qin H., et al. , The activation of OsEIL1 on YUC8 transcription and auxin biosynthesis is required for ethylene-inhibited root elongation in rice early seedling development. PLoS Genet. 13, e1006955 (2017). PubMed PMC

Zhao H., et al. , OsAUX1 controls lateral root initiation in rice (Oryza sativa L.). Plant Cell Environ. 38, 2208–2222 (2015). PubMed

Giri J., et al. , Rice auxin influx carrier OsAUX1 facilitates root hair elongation in response to low external phosphate. Nat. Commun. 9, 1408 (2018). PubMed PMC

Bulmer C. E., Simpson D. G., Soil compaction and water content as factors affecting the growth of lodgepole pine seedlings on sandy clay loam soil. Can. J. Soil Sci. 85, 667–679 (2005).

Smith C. W., et al. , The effect of soil compaction on the water retention characteristics of soils in forest plantations. S. Afr. J. Plant Soil 18, 87–97 (2001).

Woo Y. M., et al. , Constitutively wilted 1, a member of the rice YUCCA gene family, is required for maintaining water homeostasis and an appropriate root to shoot ratio. Plant Mol. Biol. 65, 125–136 (2007). PubMed

Pandey B. K., et al. , OsJAZ11 regulates phosphate starvation responses in rice. Planta 254, 8 (2021). PubMed PMC

Floková K., et al. , UHPLC-MS/MS based target profiling of stress-induced phytohormones. Phytochemistry 105, 147–157 (2014). PubMed

Dreni L., et al. , The D-lineage MADS-box gene OsMADS13 controls ovule identity in rice. Plant J. 52, 690–699 (2007). PubMed

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...