Transformation of Seed Non-Transmissible Hop Viroids in Nicotiana benthamiana Causes Distortions in Male Gametophyte Development

Viroids are small, non-coding, parasitic RNAs that promote developmental distortions in sensitive plants. We analyzed pollen of Nicotiana benthamiana after infection and/or ectopic transformation with cDNAs of citrus bark cracking viroid (CBCVd), apple fruit crinkle viroid (AFCVd)...

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Autores principales:	Lenka Steinbachová, Jaroslav Matoušek, Gerhard Steger, Helena Matoušková, Sebastjan Radišek, David Honys
Formato:	article
Lenguaje:	EN
Publicado:	MDPI AG 2021
Materias:	male gametophyte CBCVd AFCVd and PSTVd parasitic RNAs <i>Nicotiana benthamiana</i> <i>Humulus lupulus</i> plant transformation Botany QK1-989
Acceso en línea:	https://doaj.org/article/ff7e5d4361cf4b8eaba1f0bde12980ce
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spelling	oai:doaj.org-article:ff7e5d4361cf4b8eaba1f0bde12980ce2021-11-25T18:46:17ZTransformation of Seed Non-Transmissible Hop Viroids in <i>Nicotiana</i> <i>benthamiana</i> Causes Distortions in Male Gametophyte Development10.3390/plants101123982223-7747https://doaj.org/article/ff7e5d4361cf4b8eaba1f0bde12980ce2021-11-01T00:00:00Zhttps://www.mdpi.com/2223-7747/10/11/2398https://doaj.org/toc/2223-7747Viroids are small, non-coding, parasitic RNAs that promote developmental distortions in sensitive plants. We analyzed pollen of <i>Nicotiana benthamiana</i> after infection and/or ectopic transformation with cDNAs of citrus bark cracking viroid (CBCVd), apple fruit crinkle viroid (AFCVd) and potato spindle tuber viroid (PSTVd) variant AS1. These viroids were seed non-transmissible in <i>N. benthamiana</i>. All viroids propagated to high levels in immature anthers similar to leaves, while their levels were drastically reduced by approximately 3.6 × 10<sup>3</sup>, 800 and 59 times in mature pollen of CBCVd, AFCVd and PSTVd infected <i>N. benthamiana,</i> respectively, in comparison to leaves. These results suggest similar elimination processes during male gametophyte development as in the <i>Nicotiana tabacum</i> we presented in our previous study. Mature pollen of <i>N. benthamiana</i> showed no apparent defects in infected plants although all three viroids induced strong pathological symptoms on leaves. While <i>Nicotiana</i> species have naturally bicellular mature pollen, we noted a rare occurrence of mature pollen with three nuclei in CBCVd-infected <i>N. benthamiana</i>. Changes in the expression of ribosomal marker proteins in AFCVd-infected pollen were detected, suggesting some changes in pollen metabolism. <i>N. benthamiana</i> transformed with 35S-driven viroid cDNAs showed strong symptoms including defects in pollen development. A large number of aborted pollen (34% and 62%) and a slight increase of young pollen grains (8% and 15%) were found in mature pollen of AFCVd and CBCVd transformants, respectively, in comparison to control plants (3.9% aborted pollen and 0.3% young pollen). Moreover, pollen grains with malformed nuclei or trinuclear pollen were found in CBCVd-transformed plants. Our results suggest that “forcing” overexpression of seed non-transmissible viroid led to strong pollen pathogenesis. Viroid adaptation to pollen metabolism can be assumed as an important factor for viroid transmissibility through pollen and seeds.Lenka SteinbachováJaroslav MatoušekGerhard StegerHelena MatouškováSebastjan RadišekDavid HonysMDPI AGarticlemale gametophyteCBCVdAFCVd and PSTVd parasitic RNAs<i>Nicotiana benthamiana</i><i>Humulus lupulus</i>plant transformationBotanyQK1-989ENPlants, Vol 10, Iss 2398, p 2398 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	male gametophyte CBCVd AFCVd and PSTVd parasitic RNAs <i>Nicotiana benthamiana</i> <i>Humulus lupulus</i> plant transformation Botany QK1-989
spellingShingle	male gametophyte CBCVd AFCVd and PSTVd parasitic RNAs <i>Nicotiana benthamiana</i> <i>Humulus lupulus</i> plant transformation Botany QK1-989 Lenka Steinbachová Jaroslav Matoušek Gerhard Steger Helena Matoušková Sebastjan Radišek David Honys Transformation of Seed Non-Transmissible Hop Viroids in <i>Nicotiana</i> <i>benthamiana</i> Causes Distortions in Male Gametophyte Development
description	Viroids are small, non-coding, parasitic RNAs that promote developmental distortions in sensitive plants. We analyzed pollen of <i>Nicotiana benthamiana</i> after infection and/or ectopic transformation with cDNAs of citrus bark cracking viroid (CBCVd), apple fruit crinkle viroid (AFCVd) and potato spindle tuber viroid (PSTVd) variant AS1. These viroids were seed non-transmissible in <i>N. benthamiana</i>. All viroids propagated to high levels in immature anthers similar to leaves, while their levels were drastically reduced by approximately 3.6 × 10<sup>3</sup>, 800 and 59 times in mature pollen of CBCVd, AFCVd and PSTVd infected <i>N. benthamiana,</i> respectively, in comparison to leaves. These results suggest similar elimination processes during male gametophyte development as in the <i>Nicotiana tabacum</i> we presented in our previous study. Mature pollen of <i>N. benthamiana</i> showed no apparent defects in infected plants although all three viroids induced strong pathological symptoms on leaves. While <i>Nicotiana</i> species have naturally bicellular mature pollen, we noted a rare occurrence of mature pollen with three nuclei in CBCVd-infected <i>N. benthamiana</i>. Changes in the expression of ribosomal marker proteins in AFCVd-infected pollen were detected, suggesting some changes in pollen metabolism. <i>N. benthamiana</i> transformed with 35S-driven viroid cDNAs showed strong symptoms including defects in pollen development. A large number of aborted pollen (34% and 62%) and a slight increase of young pollen grains (8% and 15%) were found in mature pollen of AFCVd and CBCVd transformants, respectively, in comparison to control plants (3.9% aborted pollen and 0.3% young pollen). Moreover, pollen grains with malformed nuclei or trinuclear pollen were found in CBCVd-transformed plants. Our results suggest that “forcing” overexpression of seed non-transmissible viroid led to strong pollen pathogenesis. Viroid adaptation to pollen metabolism can be assumed as an important factor for viroid transmissibility through pollen and seeds.
format	article
author	Lenka Steinbachová Jaroslav Matoušek Gerhard Steger Helena Matoušková Sebastjan Radišek David Honys
author_facet	Lenka Steinbachová Jaroslav Matoušek Gerhard Steger Helena Matoušková Sebastjan Radišek David Honys
author_sort	Lenka Steinbachová
title	Transformation of Seed Non-Transmissible Hop Viroids in <i>Nicotiana</i> <i>benthamiana</i> Causes Distortions in Male Gametophyte Development
title_short	Transformation of Seed Non-Transmissible Hop Viroids in <i>Nicotiana</i> <i>benthamiana</i> Causes Distortions in Male Gametophyte Development
title_full	Transformation of Seed Non-Transmissible Hop Viroids in <i>Nicotiana</i> <i>benthamiana</i> Causes Distortions in Male Gametophyte Development
title_fullStr	Transformation of Seed Non-Transmissible Hop Viroids in <i>Nicotiana</i> <i>benthamiana</i> Causes Distortions in Male Gametophyte Development
title_full_unstemmed	Transformation of Seed Non-Transmissible Hop Viroids in <i>Nicotiana</i> <i>benthamiana</i> Causes Distortions in Male Gametophyte Development
title_sort	transformation of seed non-transmissible hop viroids in <i>nicotiana</i> <i>benthamiana</i> causes distortions in male gametophyte development
publisher	MDPI AG
publishDate	2021
url	https://doaj.org/article/ff7e5d4361cf4b8eaba1f0bde12980ce
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Transformation of Seed Non-Transmissible Hop Viroids in <i>Nicotiana</i> <i>benthamiana</i> Causes Distortions in Male Gametophyte Development

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