Guoqiang Huang, Azad Kilic, Michal Karady, Jiao Zhang, Poonam Mehra, Xiaoyun Song, Craig J. Sturrock, Wanwan Zhu, Hua Qin , Sjon Hartman, Hannah M. Schneider, Rahul Bhosale, Ian C. Dodd, Robert E. Sharp, Rongfeng Huang, Sacha J. Mooney, Wanqi Liang, Malcolm J. Bennett, Dabing Zhang, and Bipin K. Pandey

PNAS July 18, 2022, 119 (30) e2201072119

Significance

Intensive agriculture and changing tillage practices are causing soils to become increasingly compacted. Hard soils cause roots to accumulate the hormone ethylene, triggering reduced root elongation and increased radial swelling. We demonstrate that ethylene regulates these distinct root growth responses using different downstream signals, auxin, and abscisic acid (ABA). Auxin is primarily required to reduce cell elongation during a root compaction response, whereas ABA promotes radial cell expansion. Radial swelling was originally thought to aid root penetration in hard soil, yet rice ABA-deficient mutants disrupted in radial swelling of root tips penetrate compacted soil better than wild-type plants. The combined growth responses to auxin and ABA function to reduce the ability of roots to penetrate compacted soil.

Abstract

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.

See https://www.pnas.org/doi/10.1073/pnas.2201072119

Figure 6: Ethylene orchestrates induction of both auxin and ABA biosynthesis to regulate inhibition of elongation and promotion of radial expansion of rice roots in compacted soil. Schematic representation of root responses in (A) noncompacted soil vs. (B) compacted soil. Compacted soil conditions induce an ethylene response due to restricted outward diffusion of ethylene through smaller air-filled soil pores. Ethylene accumulation promotes OsEIL1 activation, which directly up-regulates auxin biosynthesis through OsYUC8. The enhanced auxin response in epidermal cells of meristematic and elongation zones inhibits epidermal cell elongation (and thus root elongation). In parallel, ethylene signaling promotes (indirectly) higher ABA biosynthesis in vascular tissues causing radial expansion of root cortical cells, thereby also contributing to the inhibition of root elongation in compacted soil conditions. Red dots represent gaseous ethylene molecules, red ellipse indicates enhanced ethylene response in compacted soil conditions. Intensity of color (light to darker) and width of arrow indicate higher response/level for auxin (yellow) and ABA (sky blue to royal blue). Auxin transport is denoted by green arrows.