PIP2, An Auxin Induced Plant Peptide Hormone Regulates Root and Hypocotyl Elongation in Arabidopsis.

Saddam Hussain,Tianya Wang,Yuxin Cheng,Na Zhang,Xiaojun Hu,Yating Wang,Chen Wang,Sajjad Ahmed,Siyu Chen,Shucai Wang,Xutong Wang,Adnan Adnan,Hainan Tian,Wei Wang

doi:10.3389/fpls.2021.646736

Saddam Hussain, Tianya Wang + Show 12 more

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https://doi.org/10.3389/fpls.2021.646736

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Abstract

Auxin is one of the traditional plant hormones, whereas peptide hormones are peptides with hormone activities. Both auxin and plant peptide hormones regulate multiple aspects of plant growth and development, and there are cross-talks between auxin and plant peptide hormones. PAMP-INDUCED SECRETED PEPTIDES (PIPs) and PIP-LIKEs (PIPLs) are a new family of plant peptide hormone, and PIPL3/TARGET OF LBD SIXTEEN 2 (TOLS2) has been shown to regulate lateral root formation in Arabidopsis. We report here the identification of PIP2 as an auxin response gene, and we found it plays a role in regulating root and hypocotyl development in Arabidopsis. By using quantitative RT-PCR, we found that the expression of PIP2 but not PIP1 and PIP3 was induced by auxin, and auxin induced expression of PIP2 was reduced in nph4-1 and arf19-4, the lost-of-function mutants of Auxin Response Factor 7 (ARF7) and ARF19, respectively. By generating and characterizing overexpressing transgenic lines and gene edited mutants for PIP2, we found that root length in the PIP2 overexpression plant seedlings was slightly shorter when compared with that in the Col wild type plants, but root length of the pip2 mutant seedlings remained largely unchanged. For comparison, we also generated overexpressing transgenic lines and gene edited mutants for PIP3, as well as pip2 pip3 double mutants. Surprisingly, we found that root length in the PIP3 overexpression plant seedlings is shorter than that of the PIP2 overexpression plant seedlings, and the pip3 mutant seedlings also produced short roots. However, root length in the pip2 pip3 double mutant seedlings is largely similar to that in the pip3 single mutant seedlings. On the other hand, hypocotyl elongation assays indicate that only the 35S:PIP2 transgenic plant seedlings produced longer hypocotyls when compared with the Col wild type seedlings. Further analysis indicates that PIP2 promotes cell division as well as cell elongation in hypocotyls. Taken together, our results suggest that PIP2 is an auxin response gene, and PIP2 plays a role in regulating root and hypocotyl elongation in Arabidopsis likely via regulating cell division and cell elongation.

Highlights

The plant hormone auxin regulates multiple aspects of plant growth and development largely by activating the expression of auxin response genes (Davies, 1995; Chapman and Estelle, 2009)
Unlike that observed in root elongation, seedlings of the 35S:PIP2 transgenic plant produced longer hypocotyls (Figure 6A), i.e., an ~15% longer compared with the Col wild type seedlings (Figure 6B), whereas that in the pip2 mutant seedlings remained similar to the Col wild type (Figure 6)
PIPL3, a member of the PAMP-INDUCED SECRETED PEPTIDES (PIPs) and PIPLs, a plant peptide hormone family identified in recent years (Hou et al, 2014; Vie et al, 2015), has recently shown to regulate lateral root formation (Toyokura, et al, 2019)

Summary

Introduction

The plant hormone auxin regulates multiple aspects of plant growth and development largely by activating the expression of auxin response genes (Davies, 1995; Chapman and Estelle, 2009). When the level of cellular auxin is elevated, auxin are able to bind and activate the TIR1 auxin receptor, leading to degradation of Aux/IAA proteins via 26S proteasome, release the inhibition of Aux/IAA proteins on ARF activators, resulting in activation of auxin response genes (Guilfoyle and Hagen, 2007; Tan et al, 2007; Hayashi, 2012). Exploration of the functions of the auxin response genes is still on going, as an example, the SAURs were identified as an auxin response gene family about 25 years ago (Gil et al, 1994), yet it is only in recent years that SAURs have been identified to regulate several different aspects of plant growth and development, such as cell expansion (Spartz et al, 2012; Kong et al, 2013; Qiu, et al, 2020), pollen tube growth (He et al, 2018), apical hook development (Kathare et al, 2018), hypocotyl and stamen filament elongation (Chae et al, 2012), and leaf senescence (Hou et al, 2013; Wen et al, 2020)

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