Loading…

Adaptive Reprogramming During Early Seed Germination Requires Temporarily Enhanced Fermentation-A Critical Role for Alternative Oxidase Regulation That Concerns Also Microbiota Effectiveness

Plants respond to environmental cues adaptive cell reprogramming that can affect whole plant and ecosystem functionality. Microbiota constitutes part of the inner and outer environment of the plant. This underlies steady dynamics, due to complex local and global biotic and abiotic changes. Hence, ad...

Full description

Saved in:
Bibliographic Details
Published in:Frontiers in plant science 2021-10, Vol.12, p.686274-686274
Main Authors: Bharadwaj, Revuru, Noceda, Carlos, Mohanapriya, Gunasekharan, Kumar, Sarma Rajeev, Thiers, Karine Leitão Lima, Costa, José Hélio, Macedo, Elisete Santos, Kumari, Aprajita, Gupta, Kapuganti Jagadis, Srivastava, Shivani, Adholeya, Alok, Oliveira, Manuela, Velada, Isabel, Sircar, Debabrata, Sathishkumar, Ramalingam, Arnholdt-Schmitt, Birgit
Format: Article
Language:English
Subjects:
Citations: Items that this one cites
Items that cite this one
Online Access:Get full text
Tags: Add Tag
No Tags, Be the first to tag this record!
cited_by cdi_FETCH-LOGICAL-c462t-d91c074924c4e0a6ef3a7f83efb82d6c4f8b323df58b2e58d0a41f0a52cc70953
cites cdi_FETCH-LOGICAL-c462t-d91c074924c4e0a6ef3a7f83efb82d6c4f8b323df58b2e58d0a41f0a52cc70953
container_end_page 686274
container_issue
container_start_page 686274
container_title Frontiers in plant science
container_volume 12
creator Bharadwaj, Revuru
Noceda, Carlos
Mohanapriya, Gunasekharan
Kumar, Sarma Rajeev
Thiers, Karine Leitão Lima
Costa, José Hélio
Macedo, Elisete Santos
Kumari, Aprajita
Gupta, Kapuganti Jagadis
Srivastava, Shivani
Adholeya, Alok
Oliveira, Manuela
Velada, Isabel
Sircar, Debabrata
Sathishkumar, Ramalingam
Arnholdt-Schmitt, Birgit
description Plants respond to environmental cues adaptive cell reprogramming that can affect whole plant and ecosystem functionality. Microbiota constitutes part of the inner and outer environment of the plant. This underlies steady dynamics, due to complex local and global biotic and abiotic changes. Hence, adaptive plant holobiont responses are crucial for continuous metabolic adjustment at the systems level. Plants require oxygen-dependent respiration for energy-dependent adaptive morphology, such as germination, root and shoot growth, and formation of adventitious, clonal, and reproductive organs, fruits, and seeds. Fermentative paths can help in acclimation and, to our view, the role of alternative oxidase (AOX) in coordinating complex metabolic and physiological adjustments is underestimated. Cellular levels of sucrose are an important sensor of environmental stress. We explored the role of exogenous sucrose and its interplay with AOX during early seed germination. We found that sucrose-dependent initiation of fermentation during the first 12 h after imbibition (HAI) was beneficial to germination. However, parallel upregulated expression was essential to control negative effects by prolonged sucrose treatment. Early downregulated activity until 12 HAI improved germination efficiency in the absence of sucrose but suppressed early germination in its presence. The results also suggest that seeds inoculated with arbuscular mycorrhizal fungi (AMF) can buffer sucrose stress during germination to restore normal respiration more efficiently. Following this approach, we propose a simple method to identify organic seeds and low-cost perspectives for early identifying disease tolerance, predicting plant holobiont behavior, and improving germination. Furthermore, the research strengthens the view that AOX can serve as a powerful functional marker source for seed hologenomes.
doi_str_mv 10.3389/fpls.2021.686274
format article
fullrecord <record><control><sourceid>proquest_doaj_</sourceid><recordid>TN_cdi_doaj_primary_oai_doaj_org_article_b2ef7171a44f4e3ea0d3745a1ced1619</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><doaj_id>oai_doaj_org_article_b2ef7171a44f4e3ea0d3745a1ced1619</doaj_id><sourcerecordid>2583312610</sourcerecordid><originalsourceid>FETCH-LOGICAL-c462t-d91c074924c4e0a6ef3a7f83efb82d6c4f8b323df58b2e58d0a41f0a52cc70953</originalsourceid><addsrcrecordid>eNpVkk1r3DAQhk1pacI2956Kjr3sVl-W7Uth2W7SQEog3UJvYlYe7SrYliPZoflz_W2V4zQkuozQvPPMaHiz7COjKyHK6ovtm7jilLOVKhUv5JvslCkll1Lx329f3E-ysxhvaTo5pVVVvM9OhFR5xYviNPu7rqEf3D2SG-yDPwRoW9cdyLcxTGELoXkgPxFrcoEhZWBwvkvau9EFjGSHbe8DBJdU2-4InUnK86TEbniULtdkE9zgDDTkxjdIrA9k3QwYJlRqe_3H1RCn9oexmem7Iwxk4xMrdDGJoyc_nAl-7_wAZGstmqm0wxg_ZO8sNBHPnuIi-3W-3W2-L6-uLy4366ulSRsYlnXFDC1kxaWRSEGhFVDYUqDdl7xWRtpyL7iobV7uOeZlTUEySyHnxhS0ysUiu5y5tYdb3QfXQnjQHpx-fPDhoCGkXzaoE8AWrGAgpZUoEGgtCpkDS6thilWJ9XVm9eO-xdqkVQVoXkFfZzp31Ad_r8uclSqNucg-PwGCvxsxDrp10WDTQId-jJrnpRCMK0aTlM7StL4YA9rnNozqyUV6cpGeXKRnF6WSTy_Hey747xnxD164yfE</addsrcrecordid><sourcetype>Open Website</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2583312610</pqid></control><display><type>article</type><title>Adaptive Reprogramming During Early Seed Germination Requires Temporarily Enhanced Fermentation-A Critical Role for Alternative Oxidase Regulation That Concerns Also Microbiota Effectiveness</title><source>PubMed (Medline)</source><creator>Bharadwaj, Revuru ; Noceda, Carlos ; Mohanapriya, Gunasekharan ; Kumar, Sarma Rajeev ; Thiers, Karine Leitão Lima ; Costa, José Hélio ; Macedo, Elisete Santos ; Kumari, Aprajita ; Gupta, Kapuganti Jagadis ; Srivastava, Shivani ; Adholeya, Alok ; Oliveira, Manuela ; Velada, Isabel ; Sircar, Debabrata ; Sathishkumar, Ramalingam ; Arnholdt-Schmitt, Birgit</creator><creatorcontrib>Bharadwaj, Revuru ; Noceda, Carlos ; Mohanapriya, Gunasekharan ; Kumar, Sarma Rajeev ; Thiers, Karine Leitão Lima ; Costa, José Hélio ; Macedo, Elisete Santos ; Kumari, Aprajita ; Gupta, Kapuganti Jagadis ; Srivastava, Shivani ; Adholeya, Alok ; Oliveira, Manuela ; Velada, Isabel ; Sircar, Debabrata ; Sathishkumar, Ramalingam ; Arnholdt-Schmitt, Birgit</creatorcontrib><description>Plants respond to environmental cues adaptive cell reprogramming that can affect whole plant and ecosystem functionality. Microbiota constitutes part of the inner and outer environment of the plant. This underlies steady dynamics, due to complex local and global biotic and abiotic changes. Hence, adaptive plant holobiont responses are crucial for continuous metabolic adjustment at the systems level. Plants require oxygen-dependent respiration for energy-dependent adaptive morphology, such as germination, root and shoot growth, and formation of adventitious, clonal, and reproductive organs, fruits, and seeds. Fermentative paths can help in acclimation and, to our view, the role of alternative oxidase (AOX) in coordinating complex metabolic and physiological adjustments is underestimated. Cellular levels of sucrose are an important sensor of environmental stress. We explored the role of exogenous sucrose and its interplay with AOX during early seed germination. We found that sucrose-dependent initiation of fermentation during the first 12 h after imbibition (HAI) was beneficial to germination. However, parallel upregulated expression was essential to control negative effects by prolonged sucrose treatment. Early downregulated activity until 12 HAI improved germination efficiency in the absence of sucrose but suppressed early germination in its presence. The results also suggest that seeds inoculated with arbuscular mycorrhizal fungi (AMF) can buffer sucrose stress during germination to restore normal respiration more efficiently. Following this approach, we propose a simple method to identify organic seeds and low-cost perspectives for early identifying disease tolerance, predicting plant holobiont behavior, and improving germination. Furthermore, the research strengthens the view that AOX can serve as a powerful functional marker source for seed hologenomes.</description><identifier>ISSN: 1664-462X</identifier><identifier>EISSN: 1664-462X</identifier><identifier>DOI: 10.3389/fpls.2021.686274</identifier><identifier>PMID: 34659277</identifier><language>eng</language><publisher>Switzerland: Frontiers Media S.A</publisher><subject>bacterial endophytes and mycorrhizal fungi ; biotic stress ; organic seeds ; Plant Science ; ROS ; seed quality ; Warburg effect</subject><ispartof>Frontiers in plant science, 2021-10, Vol.12, p.686274-686274</ispartof><rights>Copyright © 2021 Bharadwaj, Noceda, Mohanapriya, Kumar, Thiers, Costa, Macedo, Kumari, Gupta, Srivastava, Adholeya, Oliveira, Velada, Sircar, Sathishkumar and Arnholdt-Schmitt.</rights><rights>Copyright © 2021 Bharadwaj, Noceda, Mohanapriya, Kumar, Thiers, Costa, Macedo, Kumari, Gupta, Srivastava, Adholeya, Oliveira, Velada, Sircar, Sathishkumar and Arnholdt-Schmitt. 2021 Bharadwaj, Noceda, Mohanapriya, Kumar, Thiers, Costa, Macedo, Kumari, Gupta, Srivastava, Adholeya, Oliveira, Velada, Sircar, Sathishkumar and Arnholdt-Schmitt</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c462t-d91c074924c4e0a6ef3a7f83efb82d6c4f8b323df58b2e58d0a41f0a52cc70953</citedby><cites>FETCH-LOGICAL-c462t-d91c074924c4e0a6ef3a7f83efb82d6c4f8b323df58b2e58d0a41f0a52cc70953</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8518632/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8518632/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34659277$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Bharadwaj, Revuru</creatorcontrib><creatorcontrib>Noceda, Carlos</creatorcontrib><creatorcontrib>Mohanapriya, Gunasekharan</creatorcontrib><creatorcontrib>Kumar, Sarma Rajeev</creatorcontrib><creatorcontrib>Thiers, Karine Leitão Lima</creatorcontrib><creatorcontrib>Costa, José Hélio</creatorcontrib><creatorcontrib>Macedo, Elisete Santos</creatorcontrib><creatorcontrib>Kumari, Aprajita</creatorcontrib><creatorcontrib>Gupta, Kapuganti Jagadis</creatorcontrib><creatorcontrib>Srivastava, Shivani</creatorcontrib><creatorcontrib>Adholeya, Alok</creatorcontrib><creatorcontrib>Oliveira, Manuela</creatorcontrib><creatorcontrib>Velada, Isabel</creatorcontrib><creatorcontrib>Sircar, Debabrata</creatorcontrib><creatorcontrib>Sathishkumar, Ramalingam</creatorcontrib><creatorcontrib>Arnholdt-Schmitt, Birgit</creatorcontrib><title>Adaptive Reprogramming During Early Seed Germination Requires Temporarily Enhanced Fermentation-A Critical Role for Alternative Oxidase Regulation That Concerns Also Microbiota Effectiveness</title><title>Frontiers in plant science</title><addtitle>Front Plant Sci</addtitle><description>Plants respond to environmental cues adaptive cell reprogramming that can affect whole plant and ecosystem functionality. Microbiota constitutes part of the inner and outer environment of the plant. This underlies steady dynamics, due to complex local and global biotic and abiotic changes. Hence, adaptive plant holobiont responses are crucial for continuous metabolic adjustment at the systems level. Plants require oxygen-dependent respiration for energy-dependent adaptive morphology, such as germination, root and shoot growth, and formation of adventitious, clonal, and reproductive organs, fruits, and seeds. Fermentative paths can help in acclimation and, to our view, the role of alternative oxidase (AOX) in coordinating complex metabolic and physiological adjustments is underestimated. Cellular levels of sucrose are an important sensor of environmental stress. We explored the role of exogenous sucrose and its interplay with AOX during early seed germination. We found that sucrose-dependent initiation of fermentation during the first 12 h after imbibition (HAI) was beneficial to germination. However, parallel upregulated expression was essential to control negative effects by prolonged sucrose treatment. Early downregulated activity until 12 HAI improved germination efficiency in the absence of sucrose but suppressed early germination in its presence. The results also suggest that seeds inoculated with arbuscular mycorrhizal fungi (AMF) can buffer sucrose stress during germination to restore normal respiration more efficiently. Following this approach, we propose a simple method to identify organic seeds and low-cost perspectives for early identifying disease tolerance, predicting plant holobiont behavior, and improving germination. Furthermore, the research strengthens the view that AOX can serve as a powerful functional marker source for seed hologenomes.</description><subject>bacterial endophytes and mycorrhizal fungi</subject><subject>biotic stress</subject><subject>organic seeds</subject><subject>Plant Science</subject><subject>ROS</subject><subject>seed quality</subject><subject>Warburg effect</subject><issn>1664-462X</issn><issn>1664-462X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>DOA</sourceid><recordid>eNpVkk1r3DAQhk1pacI2956Kjr3sVl-W7Uth2W7SQEog3UJvYlYe7SrYliPZoflz_W2V4zQkuozQvPPMaHiz7COjKyHK6ovtm7jilLOVKhUv5JvslCkll1Lx329f3E-ysxhvaTo5pVVVvM9OhFR5xYviNPu7rqEf3D2SG-yDPwRoW9cdyLcxTGELoXkgPxFrcoEhZWBwvkvau9EFjGSHbe8DBJdU2-4InUnK86TEbniULtdkE9zgDDTkxjdIrA9k3QwYJlRqe_3H1RCn9oexmem7Iwxk4xMrdDGJoyc_nAl-7_wAZGstmqm0wxg_ZO8sNBHPnuIi-3W-3W2-L6-uLy4366ulSRsYlnXFDC1kxaWRSEGhFVDYUqDdl7xWRtpyL7iobV7uOeZlTUEySyHnxhS0ysUiu5y5tYdb3QfXQnjQHpx-fPDhoCGkXzaoE8AWrGAgpZUoEGgtCpkDS6thilWJ9XVm9eO-xdqkVQVoXkFfZzp31Ad_r8uclSqNucg-PwGCvxsxDrp10WDTQId-jJrnpRCMK0aTlM7StL4YA9rnNozqyUV6cpGeXKRnF6WSTy_Hey747xnxD164yfE</recordid><startdate>20211001</startdate><enddate>20211001</enddate><creator>Bharadwaj, Revuru</creator><creator>Noceda, Carlos</creator><creator>Mohanapriya, Gunasekharan</creator><creator>Kumar, Sarma Rajeev</creator><creator>Thiers, Karine Leitão Lima</creator><creator>Costa, José Hélio</creator><creator>Macedo, Elisete Santos</creator><creator>Kumari, Aprajita</creator><creator>Gupta, Kapuganti Jagadis</creator><creator>Srivastava, Shivani</creator><creator>Adholeya, Alok</creator><creator>Oliveira, Manuela</creator><creator>Velada, Isabel</creator><creator>Sircar, Debabrata</creator><creator>Sathishkumar, Ramalingam</creator><creator>Arnholdt-Schmitt, Birgit</creator><general>Frontiers Media S.A</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20211001</creationdate><title>Adaptive Reprogramming During Early Seed Germination Requires Temporarily Enhanced Fermentation-A Critical Role for Alternative Oxidase Regulation That Concerns Also Microbiota Effectiveness</title><author>Bharadwaj, Revuru ; Noceda, Carlos ; Mohanapriya, Gunasekharan ; Kumar, Sarma Rajeev ; Thiers, Karine Leitão Lima ; Costa, José Hélio ; Macedo, Elisete Santos ; Kumari, Aprajita ; Gupta, Kapuganti Jagadis ; Srivastava, Shivani ; Adholeya, Alok ; Oliveira, Manuela ; Velada, Isabel ; Sircar, Debabrata ; Sathishkumar, Ramalingam ; Arnholdt-Schmitt, Birgit</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c462t-d91c074924c4e0a6ef3a7f83efb82d6c4f8b323df58b2e58d0a41f0a52cc70953</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>bacterial endophytes and mycorrhizal fungi</topic><topic>biotic stress</topic><topic>organic seeds</topic><topic>Plant Science</topic><topic>ROS</topic><topic>seed quality</topic><topic>Warburg effect</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Bharadwaj, Revuru</creatorcontrib><creatorcontrib>Noceda, Carlos</creatorcontrib><creatorcontrib>Mohanapriya, Gunasekharan</creatorcontrib><creatorcontrib>Kumar, Sarma Rajeev</creatorcontrib><creatorcontrib>Thiers, Karine Leitão Lima</creatorcontrib><creatorcontrib>Costa, José Hélio</creatorcontrib><creatorcontrib>Macedo, Elisete Santos</creatorcontrib><creatorcontrib>Kumari, Aprajita</creatorcontrib><creatorcontrib>Gupta, Kapuganti Jagadis</creatorcontrib><creatorcontrib>Srivastava, Shivani</creatorcontrib><creatorcontrib>Adholeya, Alok</creatorcontrib><creatorcontrib>Oliveira, Manuela</creatorcontrib><creatorcontrib>Velada, Isabel</creatorcontrib><creatorcontrib>Sircar, Debabrata</creatorcontrib><creatorcontrib>Sathishkumar, Ramalingam</creatorcontrib><creatorcontrib>Arnholdt-Schmitt, Birgit</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>Directory of Open Access Journals</collection><jtitle>Frontiers in plant science</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Bharadwaj, Revuru</au><au>Noceda, Carlos</au><au>Mohanapriya, Gunasekharan</au><au>Kumar, Sarma Rajeev</au><au>Thiers, Karine Leitão Lima</au><au>Costa, José Hélio</au><au>Macedo, Elisete Santos</au><au>Kumari, Aprajita</au><au>Gupta, Kapuganti Jagadis</au><au>Srivastava, Shivani</au><au>Adholeya, Alok</au><au>Oliveira, Manuela</au><au>Velada, Isabel</au><au>Sircar, Debabrata</au><au>Sathishkumar, Ramalingam</au><au>Arnholdt-Schmitt, Birgit</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Adaptive Reprogramming During Early Seed Germination Requires Temporarily Enhanced Fermentation-A Critical Role for Alternative Oxidase Regulation That Concerns Also Microbiota Effectiveness</atitle><jtitle>Frontiers in plant science</jtitle><addtitle>Front Plant Sci</addtitle><date>2021-10-01</date><risdate>2021</risdate><volume>12</volume><spage>686274</spage><epage>686274</epage><pages>686274-686274</pages><issn>1664-462X</issn><eissn>1664-462X</eissn><abstract>Plants respond to environmental cues adaptive cell reprogramming that can affect whole plant and ecosystem functionality. Microbiota constitutes part of the inner and outer environment of the plant. This underlies steady dynamics, due to complex local and global biotic and abiotic changes. Hence, adaptive plant holobiont responses are crucial for continuous metabolic adjustment at the systems level. Plants require oxygen-dependent respiration for energy-dependent adaptive morphology, such as germination, root and shoot growth, and formation of adventitious, clonal, and reproductive organs, fruits, and seeds. Fermentative paths can help in acclimation and, to our view, the role of alternative oxidase (AOX) in coordinating complex metabolic and physiological adjustments is underestimated. Cellular levels of sucrose are an important sensor of environmental stress. We explored the role of exogenous sucrose and its interplay with AOX during early seed germination. We found that sucrose-dependent initiation of fermentation during the first 12 h after imbibition (HAI) was beneficial to germination. However, parallel upregulated expression was essential to control negative effects by prolonged sucrose treatment. Early downregulated activity until 12 HAI improved germination efficiency in the absence of sucrose but suppressed early germination in its presence. The results also suggest that seeds inoculated with arbuscular mycorrhizal fungi (AMF) can buffer sucrose stress during germination to restore normal respiration more efficiently. Following this approach, we propose a simple method to identify organic seeds and low-cost perspectives for early identifying disease tolerance, predicting plant holobiont behavior, and improving germination. Furthermore, the research strengthens the view that AOX can serve as a powerful functional marker source for seed hologenomes.</abstract><cop>Switzerland</cop><pub>Frontiers Media S.A</pub><pmid>34659277</pmid><doi>10.3389/fpls.2021.686274</doi><tpages>1</tpages><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 1664-462X
ispartof Frontiers in plant science, 2021-10, Vol.12, p.686274-686274
issn 1664-462X
1664-462X
language eng
recordid cdi_doaj_primary_oai_doaj_org_article_b2ef7171a44f4e3ea0d3745a1ced1619
source PubMed (Medline)
subjects bacterial endophytes and mycorrhizal fungi
biotic stress
organic seeds
Plant Science
ROS
seed quality
Warburg effect
title Adaptive Reprogramming During Early Seed Germination Requires Temporarily Enhanced Fermentation-A Critical Role for Alternative Oxidase Regulation That Concerns Also Microbiota Effectiveness
url http://sfxeu10.hosted.exlibrisgroup.com/loughborough?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-24T23%3A27%3A19IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_doaj_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Adaptive%20Reprogramming%20During%20Early%20Seed%20Germination%20Requires%20Temporarily%20Enhanced%20Fermentation-A%20Critical%20Role%20for%20Alternative%20Oxidase%20Regulation%20That%20Concerns%20Also%20Microbiota%20Effectiveness&rft.jtitle=Frontiers%20in%20plant%20science&rft.au=Bharadwaj,%20Revuru&rft.date=2021-10-01&rft.volume=12&rft.spage=686274&rft.epage=686274&rft.pages=686274-686274&rft.issn=1664-462X&rft.eissn=1664-462X&rft_id=info:doi/10.3389/fpls.2021.686274&rft_dat=%3Cproquest_doaj_%3E2583312610%3C/proquest_doaj_%3E%3Cgrp_id%3Ecdi_FETCH-LOGICAL-c462t-d91c074924c4e0a6ef3a7f83efb82d6c4f8b323df58b2e58d0a41f0a52cc70953%3C/grp_id%3E%3Coa%3E%3C/oa%3E%3Curl%3E%3C/url%3E&rft_id=info:oai/&rft_pqid=2583312610&rft_id=info:pmid/34659277&rfr_iscdi=true