@article{mazzoni-putman_brumos_zhao_alonso_stepanova_2021, title={Auxin Interactions with Other Hormones in Plant Development}, volume={13}, ISSN={1943-0264}, url={http://dx.doi.org/10.1101/cshperspect.a039990}, DOI={10.1101/cshperspect.a039990}, abstractNote={Auxin is a crucial growth regulator that governs plant development and responses to environmental perturbations. It functions at the heart of many developmental processes, from embryogenesis to organ senescence, and is key to plant interactions with the environment, including responses to biotic and abiotic stimuli. As remarkable as auxin is, it does not act alone, but rather solicits the help of, or is solicited by, other endogenous signals, including the plant hormones abscisic acid, brassinosteroids, cytokinins, ethylene, gibberellic acid, jasmonates, salicylic acid, and strigolactones. The interactions between auxin and other hormones occur at multiple levels: hormones regulate one another's synthesis, transport, and/or response; hormone-specific transcriptional regulators for different pathways physically interact and/or converge on common target genes; etc. However, our understanding of this crosstalk is still fragmentary, with only a few pieces of the gigantic puzzle firmly established. In this review, we provide a glimpse into the complexity of hormone interactions that involve auxin, underscoring how patchy our current understanding is.}, number={10}, journal={Cold Spring Harbor Perspectives in Biology}, publisher={Cold Spring Harbor Laboratory}, author={Mazzoni-Putman, Serina M. and Brumos, Javier and Zhao, Chengsong and Alonso, Jose M. and Stepanova, Anna N.}, year={2021}, month={Apr}, pages={a039990} }
 @article{agusti_ramireddy_brumos_2021, title={Editorial: Integration of Hormonal Signals Shaping Root Growth, Development, and Architecture}, volume={12}, ISSN={["1664-462X"]}, DOI={10.3389/fpls.2021.634066}, abstractNote={EDITORIAL article Front. Plant Sci., 12 February 2021 | https://doi.org/10.3389/fpls.2021.634066}, journal={FRONTIERS IN PLANT SCIENCE}, author={Agusti, Javier and Ramireddy, Eswarayya and Brumos, Javier}, year={2021}, month={Feb} }
 @article{brumos_robles_yun_vu_jackson_alonso_stepanova_2018, title={Local Auxin Biosynthesis Is a Key Regulator of Plant Development}, volume={47}, ISSN={["1878-1551"]}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-85055097260&partnerID=MN8TOARS}, DOI={10.1016/j.devcel.2018.09.022}, abstractNote={•Local auxin production in roots is required for maintaining functional root meristems•Local biosynthesis and transport of auxin cooperate at generating robust auxin maxima•Auxin produced in the root quiescent center is sufficient for root meristem viability Auxin is a major phytohormone that controls numerous aspects of plant development and coordinates plant responses to the environment. Morphogenic gradients of auxin govern cell fate decisions and underlie plant phenotypic plasticity. Polar auxin transport plays a central role in auxin maxima generation. The discovery of the exquisite spatiotemporal expression patterns of auxin biosynthesis genes of the WEI8/TAR and YUC families suggested that local auxin production may contribute to the formation of auxin maxima. Herein, we systematically addressed the role of local auxin biosynthesis in plant development and responses to the stress phytohormone ethylene by manipulating spatiotemporal patterns of WEI8. Our study revealed that local auxin biosynthesis and transport act synergistically and are individually dispensable for root meristem maintenance. In contrast, flower fertility and root responses to ethylene require local auxin production that cannot be fully compensated for by transport in the generation of morphogenic auxin maxima. Auxin is a major phytohormone that controls numerous aspects of plant development and coordinates plant responses to the environment. Morphogenic gradients of auxin govern cell fate decisions and underlie plant phenotypic plasticity. Polar auxin transport plays a central role in auxin maxima generation. The discovery of the exquisite spatiotemporal expression patterns of auxin biosynthesis genes of the WEI8/TAR and YUC families suggested that local auxin production may contribute to the formation of auxin maxima. Herein, we systematically addressed the role of local auxin biosynthesis in plant development and responses to the stress phytohormone ethylene by manipulating spatiotemporal patterns of WEI8. Our study revealed that local auxin biosynthesis and transport act synergistically and are individually dispensable for root meristem maintenance. In contrast, flower fertility and root responses to ethylene require local auxin production that cannot be fully compensated for by transport in the generation of morphogenic auxin maxima. Nearly every aspect of a plant’s life is influenced by auxin. Not only does this phytohormone govern many developmental programs of the plant but also is able to tune plant growth and development according to the ever-changing external conditions surrounding the plant. In the meristems, auxin regulates cell division, elongation, and differentiation leading to downstream organogenesis that shapes shoot and root architecture. The vital roles of auxin gradients in plant growth and development have been established and interpreted mainly as the product of the combined action of auxin transport, signaling and response. Conversely, little is known about the contribution of the de novo auxin biosynthesis to the generation and maintenance of the morphogenic auxin maxima. A thorough understanding of how and where auxin is produced is nonetheless critical to our ability to precisely define auxin sources and sinks and thereby to establish a more refined picture of the polar transport system and auxin activity. It is only in the past 20 years that a combination of genetic, biochemical, and pharmacological approaches (Zhao et al., 2001Zhao Y. Christensen S.K. Fankhauser C. Cashman J.R. Cohen J.D. Weigel D. Chory J. A role for flavin monooxygenase-like enzymes in auxin biosynthesis.Science. 2001; 291: 306-309Crossref PubMed Scopus (868) Google Scholar, Cheng et al., 2006Cheng Y. Dai X. Zhao Y. Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis.Genes Dev. 2006; 20: 1790-1799Crossref PubMed Scopus (808) Google Scholar, Cheng et al., 2007Cheng Y. Dai X. Zhao Y. Auxin synthesized by the YUCCA flavin monooxygenases is essential for embryogenesis and leaf formation in Arabidopsis.Plant Cell. 2007; 19: 2430-2439Crossref PubMed Scopus (474) Google Scholar, Stepanova et al., 2008Stepanova A.N. Robertson-Hoyt J. Yun J. Benavente L.M. Xie D.Y. Dolezal K. Schlereth A. Jürgens G. Alonso J.M. TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development.Cell. 2008; 133: 177-191Abstract Full Text Full Text PDF PubMed Scopus (793) Google Scholar, Tao et al., 2008Tao Y. Ferrer J. Ljung K. Pojer F. Hong F. Long J.A. Li L. Moreno J.E. Bowman M.E. Ivans L.J. et al.Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants.Cell. 2008; 133: 164-176Abstract Full Text Full Text PDF PubMed Scopus (753) Google Scholar, Mashiguchi et al., 2011Mashiguchi K. Tanaka K. Sakai T. Sugawara S. Kawaide H. Natsume M. Hanada A. Yaeno T. Shirasu K. Yao H. et al.The main auxin biosynthesis pathway in Arabidopsis.Proc. Natl. Acad. Sci. USA. 2011; 108: 18512-18517Crossref PubMed Scopus (629) Google Scholar, Stepanova et al., 2011Stepanova A.N. Yun J. Robles L.M. Novak O. He W. Guo H. Ljung K. Alonso J.M. The Arabidopsis YUCCA1 flavin monooxygenase functions in the indole-3-pyruvic acid branch of auxin biosynthesis.Plant Cell. 2011; 23: 3961-3973Crossref PubMed Scopus (260) Google Scholar), together with the development of more sensitive methodologies for auxin metabolite quantification (Novák et al., 2012Novák O. Hényková E. Sairanen I. Kowalczyk M. Pospíšil T. Ljung K. Tissue-specific profiling of the Arabidopsis thaliana auxin metabolome.Plant J. 2012; 72: 523-536Crossref PubMed Scopus (207) Google Scholar), have led to the identification of the first complete pathway of auxin biosynthesis in plants. The best characterized auxin in plants, indole-3-acetic acid (IAA), is predominantly produced from the aromatic amino acid L-tryptophan (Trp) via indole-3-pyruvic acid (IPyA) in a two-step pathway (reviewed in Brumos et al., 2014Brumos J. Alonso J.M. Stepanova A.N. Genetic aspects of auxin biosynthesis and its regulation.Physiol. Plant. 2014; 151: 3-12Crossref PubMed Scopus (62) Google Scholar). Trp is first converted to IPyA by a small family of tryptophan aminotransferases that in Arabidopsis is represented by TRYPTOPHAN AMINOTRANSFERASE OF ARABIDOPSIS1 (TAA1) (also known as WEAK ETHYLENE INSENSITIVE8 [WEI8] [Stepanova et al., 2008Stepanova A.N. Robertson-Hoyt J. Yun J. Benavente L.M. Xie D.Y. Dolezal K. Schlereth A. Jürgens G. Alonso J.M. TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development.Cell. 2008; 133: 177-191Abstract Full Text Full Text PDF PubMed Scopus (793) Google Scholar], SHADE AVOIDANCE3 [SAV3] [Tao et al., 2008Tao Y. Ferrer J. Ljung K. Pojer F. Hong F. Long J.A. Li L. Moreno J.E. Bowman M.E. Ivans L.J. et al.Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants.Cell. 2008; 133: 164-176Abstract Full Text Full Text PDF PubMed Scopus (753) Google Scholar], TRANSPORT INHIBITOR RESPONSE2 [TIR2] [Yamada et al., 2009Yamada M. Greenham K. Prigge M.J. Jensen P.J. Estelle M. The TRANSPORT INHIBITOR RESPONSE2 gene is required for auxin synthesis and diverse aspects of plant development.Plant Physiol. 2009; 151: 168-179Crossref PubMed Scopus (144) Google Scholar], and CYTOKININ INDUCED ROOT CURLING1 [CKRC1] [Zhou et al., 2011Zhou Z.Y. Zhang C.G. Wu L. Zhang C.G. Chai J. Wang M. Jha A. Jia P.F. Cui S.J. Yang M. et al.Functional characterization of the CKRC1/TAA1 gene and dissection of hormonal actions in the Arabidopsis root.Plant J. 2011; 66: 516-527Crossref PubMed Scopus (54) Google Scholar]) and its paralogs TRYPTOPHAN AMINOTRANSFERASE RELATED1 (TAR1) and TAR2 (Stepanova et al., 2008Stepanova A.N. Robertson-Hoyt J. Yun J. Benavente L.M. Xie D.Y. Dolezal K. Schlereth A. Jürgens G. Alonso J.M. TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development.Cell. 2008; 133: 177-191Abstract Full Text Full Text PDF PubMed Scopus (793) Google Scholar). IPyA is then converted into IAA by the YUCCA (YUC) family of flavin monooxygenases that in Arabidopsis consists of 11 members, YUC1 through YUC11 (reviewed in Zhao, 2014Zhao Y. Auxin biosynthesis.in: The Arabidopsis Book. American Society of Plant Biologists, 2014: e0173Crossref Google Scholar). According to the classical view in the auxin field, a majority of auxin in plants is produced in the shoot apical meristems, young leaves, and flower buds and is rapidly distributed throughout the plant via the phloem (reviewed in Teale et al., 2006Teale W.D. Paponov I.A. Palme K. Auxin in action: signalling, transport and the control of plant growth and development.Nat. Rev. Mol. Cell Biol. 2006; 7: 847-859Crossref PubMed Scopus (848) Google Scholar). In addition, auxin can move more slowly cell to cell via polar auxin transport with the help of auxin influx carriers AUXIN1 (AUX1)/LIKE-AUXs (LAXs) and auxin efflux transporters PIN FORMED (PINs) and ABCB/MULTIDRUG RESISTANCE (MDR)/PHOSPHOGLYCOPROTEIN (PGPs) (reviewed in Adamowski and Friml, 2015Adamowski M. Friml J. PIN-dependent auxin transport: action, regulation, and evolution.Plant Cell. 2015; 27: 20-32Crossref PubMed Scopus (460) Google Scholar). It is the polar distribution of PINs within cells that is thought to enable directional flow of auxin to generate robust morphogenic auxin gradients that instruct plant development. The classical view has however been challenged by the finding that auxin can also be synthesized locally in roots (Ljun et al., 2002Ljung K. Hul A.K. Kowalczyk M. Marchant A. Celenza J. Cohen J.D. Sandberg G. Biosynthesis, conjugation, catabolism and homeostasis of indole-3-acetic acid in Arabidopsis thaliana.Plant Mol. Biol. 2002; 50: 309-332Crossref PubMed Scopus (126) Google Scholar, Ljung et al., 2005Ljung K. Hull A.K. Celenza J. Yamada M. Estelle M. Normanly J. Sandberg G. Sites and regulation of auxin biosynthesis in Arabidopsis roots.Plant Cell. 2005; 17: 1090-1104Crossref PubMed Scopus (409) Google Scholar, Stepanova et al., 2008Stepanova A.N. Robertson-Hoyt J. Yun J. Benavente L.M. Xie D.Y. Dolezal K. Schlereth A. Jürgens G. Alonso J.M. TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development.Cell. 2008; 133: 177-191Abstract Full Text Full Text PDF PubMed Scopus (793) Google Scholar). Cloning of the auxin biosynthesis genes WEI8/TARs and YUCs uncovered that they are expressed not only in shoots but also in roots, and the domains of expression of several of these genes coincide with the auxin response maxima in root tips (Stepanova et al., 2008Stepanova A.N. Robertson-Hoyt J. Yun J. Benavente L.M. Xie D.Y. Dolezal K. Schlereth A. Jürgens G. Alonso J.M. TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development.Cell. 2008; 133: 177-191Abstract Full Text Full Text PDF PubMed Scopus (793) Google Scholar, Chen et al., 2014Chen Q. Dai X. De-Paoli H. Cheng Y. Takebayashi Y. Kasahara H. Kamiya Y. Zhao Y. Auxin overproduction in shoots cannot rescue auxin deficiencies in Arabidopsis roots.Plant Cell Physiol. 2014; 55: 1072-1079Crossref PubMed Scopus (142) Google Scholar), as defined by the auxin activity reporters DR5:GFP or DII-VENUS (Ulmasov et al., 1997Ulmasov T. Murfett J. Hagen G. Guilfoyle T.J. Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements.Plant Cell. 1997; 9: 1963-1971Crossref PubMed Scopus (1591) Google Scholar, Brunoud et al., 2012Brunoud G. Wells D.M. Oliva M. Larrieu A. Mirabet V. Burrow A.H. Beeckman T. Kepinski S. Traas J. Bennett M.J. et al.A novel sensor to map auxin response and distribution at high spatio-temporal resolution.Nature. 2012; 482: 103-106Crossref PubMed Scopus (528) Google Scholar, Liao et al., 2015Liao C.Y. Smet W. Brunoud G. Yoshida S. Vernoux T. Weijers D. Reporters for sensitive and quantitative measurement of auxin response.Nat. Methods. 2015; 12: 207-210Crossref PubMed Scopus (245) Google Scholar). Multiple higher order wei8/tar and yuc mutants show dramatic developmental effects (Stepanova et al., 2008Stepanova A.N. Robertson-Hoyt J. Yun J. Benavente L.M. Xie D.Y. Dolezal K. Schlereth A. Jürgens G. Alonso J.M. TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development.Cell. 2008; 133: 177-191Abstract Full Text Full Text PDF PubMed Scopus (793) Google Scholar, Tao et al., 2008Tao Y. Ferrer J. Ljung K. Pojer F. Hong F. Long J.A. Li L. Moreno J.E. Bowman M.E. Ivans L.J. et al.Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants.Cell. 2008; 133: 164-176Abstract Full Text Full Text PDF PubMed Scopus (753) Google Scholar, Cheng et al., 2007Cheng Y. Dai X. Zhao Y. Auxin synthesized by the YUCCA flavin monooxygenases is essential for embryogenesis and leaf formation in Arabidopsis.Plant Cell. 2007; 19: 2430-2439Crossref PubMed Scopus (474) Google Scholar, Cheng et al., 2006Cheng Y. Dai X. Zhao Y. Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis.Genes Dev. 2006; 20: 1790-1799Crossref PubMed Scopus (808) Google Scholar), suggesting that local activity of the biosynthesis genes may have a direct role in the generation and/or maintenance of auxin maxima. Supporting the key role of local biosynthesis is the finding that auxin produced in the aerial parts of plants is unable to compensate for an auxin biosynthesis deficiency of yucQ mutants in roots, resulting in the degeneration of root meristems (Chen et al., 2014Chen Q. Dai X. De-Paoli H. Cheng Y. Takebayashi Y. Kasahara H. Kamiya Y. Zhao Y. Auxin overproduction in shoots cannot rescue auxin deficiencies in Arabidopsis roots.Plant Cell Physiol. 2014; 55: 1072-1079Crossref PubMed Scopus (142) Google Scholar). The discovery of an essential contribution of locally made auxin to PIN polarization and to the establishment of the apical-basal axis in young embryos further implicates tissue-specific auxin production in the control of plant development (Robert et al., 2013Robert H.S. Grones P. Stepanova A.N. Robles L.M. Lokerse A.S. Alonso J.M. Weijers D. Friml J. Local auxin sources orient the apical-basal axis in Arabidopsis embryos.Curr. Biol. 2013; 23: 2506-2512Abstract Full Text Full Text PDF PubMed Scopus (148) Google Scholar). Thus, in some developmental contexts, the location of auxin sources is of critical physiological importance, and long-distance transport may not suffice for the generation of morphogenetic auxin gradients in all tissues. On the other hand, a uniform supply of IAA in the growth medium can partially suppress the root meristem defects of strong auxin biosynthetic mutants (Stepanova et al., 2011Stepanova A.N. Yun J. Robles L.M. Novak O. He W. Guo H. Ljung K. Alonso J.M. The Arabidopsis YUCCA1 flavin monooxygenase functions in the indole-3-pyruvic acid branch of auxin biosynthesis.Plant Cell. 2011; 23: 3961-3973Crossref PubMed Scopus (260) Google Scholar), suggesting that a non-localized source of auxin readily available to roots may be all that is needed for the transport machinery to generate the auxin maxima required for root development. Consistent with the latter argument are the conclusions of the first experimental and mathematical modeling approaches that showed how the auxin transport system alone could generate robust auxin gradients in roots with any (i.e., non-local) sources of auxin (Grieneisen et al., 2007Grieneisen V.A. Xu J. Marée A.F.M. Hogeweg P. Scheres B. Auxin transport is sufficient to generate a maximum and gradient guiding root growth.Nature. 2007; 449: 1008-1013Crossref PubMed Scopus (626) Google Scholar). Alternative models were later built under the assumption that minor production and degradation of auxin do take place in every root cell, but higher auxin production rates occur in the quiescent center (QC) and columella initials to account for the local synthesis of auxin in the root meristem (Band et al., 2014Band L.R. Wells D.M. Fozard J.A. Ghetiu T. French A.P. Pound M.P. Wilson M.H. Yu L. Li W. Hijazi H.I. et al.Systems analysis of auxin transport in the Arabidopsis root apex.Plant Cell. 2014; 26: 862-875Crossref PubMed Scopus (147) Google Scholar). If locally made auxin was removed from these models, the gradient was not qualitatively affected (Band et al., 2014Band L.R. Wells D.M. Fozard J.A. Ghetiu T. French A.P. Pound M.P. Wilson M.H. Yu L. Li W. Hijazi H.I. et al.Systems analysis of auxin transport in the Arabidopsis root apex.Plant Cell. 2014; 26: 862-875Crossref PubMed Scopus (147) Google Scholar), arguing against the crucial role of local sources of auxin. These modeling experiments, however, made an assumption that all root cells make some auxin, which is not in agreement with the highly restricted expression patterns of the WEI8/TAR family in roots (Stepanova et al., 2008Stepanova A.N. Robertson-Hoyt J. Yun J. Benavente L.M. Xie D.Y. Dolezal K. Schlereth A. Jürgens G. Alonso J.M. TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development.Cell. 2008; 133: 177-191Abstract Full Text Full Text PDF PubMed Scopus (793) Google Scholar). Thus, the relative contributions of local auxin production and transport, both long and short distance, remain largely undefined, warranting the need for further inquiry into the potentially overlapping roles of the biosynthesis and transport of this hormone. Both auxin biosynthesis and transport regulate plant development not only under optimal laboratory conditions but also in response to a stress hormone ethylene (Růzicka et al., 2007Růzicka K. Ljung K. Vanneste S. Podhorská R. Beeckman T. Friml J. Benková E. Ethylene regulates root growth through effects on auxin biosynthesis and transport-dependent auxin distribution.Plant Cell. 2007; 19: 2197-2212Crossref PubMed Scopus (575) Google Scholar, Swarup et al., 2007Swarup R. Perry P. Hagenbeek D. Van Der Straeten D. Beemster G.T. Sandberg G. Bhalerao R.P. Ljung K. Bennett M.J. Ethylene upregulates auxin biosynthesis in Arabidopsis seedlings to enhance inhibition of root cell elongation.Plant Cell. 2007; 19: 2186-2196Crossref PubMed Scopus (457) Google Scholar, Stepanova et al., 2007Stepanova A.N. Yun J. Likhacheva A.V. Alonso J.M. Multilevel interactions between ethylene and auxin in Arabidopsis roots.Plant Cell. 2007; 19: 2169-2185Crossref PubMed Scopus (410) Google Scholar, Stepanova et al., 2008Stepanova A.N. Robertson-Hoyt J. Yun J. Benavente L.M. Xie D.Y. Dolezal K. Schlereth A. Jürgens G. Alonso J.M. TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development.Cell. 2008; 133: 177-191Abstract Full Text Full Text PDF PubMed Scopus (793) Google Scholar). Exposure of plants to ethylene or its precursor ACC is known to trigger specific patterns of local auxin production, transport, and response in roots of Arabidopsis seedlings by stimulating transcription of auxin biosynthesis and transport genes (Růzicka et al., 2007Růzicka K. Ljung K. Vanneste S. Podhorská R. Beeckman T. Friml J. Benková E. Ethylene regulates root growth through effects on auxin biosynthesis and transport-dependent auxin distribution.Plant Cell. 2007; 19: 2197-2212Crossref PubMed Scopus (575) Google Scholar, Swarup et al., 2007Swarup R. Perry P. Hagenbeek D. Van Der Straeten D. Beemster G.T. Sandberg G. Bhalerao R.P. Ljung K. Bennett M.J. Ethylene upregulates auxin biosynthesis in Arabidopsis seedlings to enhance inhibition of root cell elongation.Plant Cell. 2007; 19: 2186-2196Crossref PubMed Scopus (457) Google Scholar, Stepanova et al., 2007Stepanova A.N. Yun J. Likhacheva A.V. Alonso J.M. Multilevel interactions between ethylene and auxin in Arabidopsis roots.Plant Cell. 2007; 19: 2169-2185Crossref PubMed Scopus (410) Google Scholar, Stepanova et al., 2008Stepanova A.N. Robertson-Hoyt J. Yun J. Benavente L.M. Xie D.Y. Dolezal K. Schlereth A. Jürgens G. Alonso J.M. TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development.Cell. 2008; 133: 177-191Abstract Full Text Full Text PDF PubMed Scopus (793) Google Scholar). Not surprisingly, genetic defects in the numerous components of the auxin biosynthesis, transport, perception, or response machineries (Merchante and Stepanova, 2017Merchante C. Stepanova A.N. The triple response assay and its use to characterize ethylene mutants in Arabidopsis.Methods Mol. Biol. 2017; 1573: 163-209Crossref Scopus (14) Google Scholar) lead to root-specific ethylene insensitivity. These findings suggest that auxin production and transport and, consequently, proper levels of auxin signaling and response are prerequisites for normal responses of Arabidopsis roots to ethylene and provide a convenient platform for elucidating the respective roles of auxin biosynthesis and transport in a physiologically relevant context. Herein, we evaluated the contribution of localized auxin production versus polar transport to specific growth and development programs in Arabidopsis. Our data indicate that root-produced local sources of auxin are required for root stem cell niche maintenance, whereas shoot-derived auxin alone cannot keep the root meristems alive. Local auxin biosynthesis and auxin transport in roots act redundantly in the establishment and maintenance of robust morphogenetic maxima critical for root meristem activity. In contrast, local auxin biosynthesis is essential (and cannot be fully compensated for by transport) for root responses to hormone ethylene, as well as for flower development. Thus, local auxin production and transport in plants represent partially redundant physiological mechanisms that work together to confer greater robustness and tunability to instructional auxin gradients, enabling developmental plasticity and adaptation of plants to changing environmental conditions. Prior studies (Stepanova et al., 2008Stepanova A.N. Robertson-Hoyt J. Yun J. Benavente L.M. Xie D.Y. Dolezal K. Schlereth A. Jürgens G. Alonso J.M. TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development.Cell. 2008; 133: 177-191Abstract Full Text Full Text PDF PubMed Scopus (793) Google Scholar) demonstrated that in wei8 tar2 a deficiency in auxin synthesized via the IPyA pathway results in a loss of robust auxin gradients and leads to root meristem degeneration. Herein, to dissect the role of shoot- versus root-derived auxin in root meristem maintenance, we performed reciprocal grafting of shoots and roots of wild-type (WT) and wei8 tar2 seedlings introgressed with an auxin-responsive reporter DR5:GFP at 3 days post germination, i.e., prior to mutant seedlings displaying any obvious signs of root stem cell loss (Stepanova et al., 2008Stepanova A.N. Robertson-Hoyt J. Yun J. Benavente L.M. Xie D.Y. Dolezal K. Schlereth A. Jürgens G. Alonso J.M. TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development.Cell. 2008; 133: 177-191Abstract Full Text Full Text PDF PubMed Scopus (793) Google Scholar), and examined DR5:GFP activity 1 week and 3 weeks after the surgery (Figures 1A and S1A). WT shoots grafted onto the mutant roots (WT/wei8 tar2) did not prevent root meristem degeneration, suggesting that WT shoot sources of auxin could not compensate for the auxin deficiency in roots and that auxin produced locally in roots is critical for root meristem health. One can argue that in these plants the vasculature may reconnect too late for the shoot-derived auxin to reach the root tip on time and prevent wei8 tar2 root meristem degeneration. Indeed, although the phloem of grafted WT plants reconnects within 3 days of grafting (Melnyk et al., 2015Melnyk C.W. Schuster C. Leyser O. Meyerowitz E.M. A developmental framework for graft formation and vascular reconnection in Arabidopsis thaliana.Curr. Biol. 2015; 25: 1306-1318Abstract Full Text Full Text PDF PubMed Scopus (165) Google Scholar), the process may take longer in grafts involving the compromised wei8 tar2 vasculature, and the meristematic potential of wei8 tar2 roots does decline over time (see below). Nonetheless, WT roots that received mutant shoots (wei8 tar2/WT) maintained healthy root meristems with normal patterns of DR5:GFP (Figure 1A), implying that local supply of auxin is necessary for root stem cell niche maintenance. One caveat of this experiment is that the shoots of wei8 tar2 are not completely devoid of auxin (Stepanova et al., 2008Stepanova A.N. Robertson-Hoyt J. Yun J. Benavente L.M. Xie D.Y. Dolezal K. Schlereth A. Jürgens G. Alonso J.M. TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development.Cell. 2008; 133: 177-191Abstract Full Text Full Text PDF PubMed Scopus (793) Google Scholar), and thus, the possibility that in these grafted plants some shoot auxin did travel to the roots cannot be discarded. On the other hand, auxin locally produced in WT roots of wei8 tar2/WT grafted plants was not sufficient to reverse the morphological defects of wei8 tar2 shoots (Figure S1B). Control experiments with WT/WT grafts resulted in normal DR5:GFP expression in roots, whereas wei8 tar2/wei8 tar2 grafts lost their DR5:GFP and root meristem activity (Figure 1A). Additional controls using detached roots showed root degeneration and loss of DR5:GFP activity (Figure S1A). These results are consistent with the notion that local auxin produced in roots is required for root meristem activity. Likewise, shoots but not necessarily shoot-derived auxin are needed for root survival. To differentiate between the roles of shoot versus root sources of auxin in root meristem maintenance, we next employed a heat shock-inducible Cre/Lox auxin production system (Figure S1C) (Dubrovsky et al., 2008Dubrovsky J.G. Sauer M. Napsucialy-Mendivil S. Ivanchenko M.G. Friml J. Shishkova S. Celenza J. Benková E. Auxin acts as a local morphogenetic trigger to specify lateral root founder cells.Proc. Natl. Acad. Sci. USA. 2008; 105: 8790-8794Crossref PubMed Scopus (444) Google Scholar). This system turns on a bacterial auxin biosynthesis enzyme, iaaM, upon exposure of plants to heat stress, and the activation of the system can be monitored by GUS staining. We amended the system by introducing another bacterial auxin biosynthesis gene, iaaH, into the plants that harbor the Cre≫iaaM/GUS system to insure rapid and efficient auxin production independent of the endogenous plant pathways (Figure S1C). We triggered auxin synthesis in shoots or in roots by exposing the above- or below-ground parts of seedlings to high temperatures and monitored the effectiveness of the treatment by relying on GUS activity (Figures 1B and S1D). To eliminate the effect of the major endogenous pathway of auxin biosynthesis, we applied a combination of kynurenine (an inhibitor of TAA1/TARs) and yucasin (an inhibitor of YUCs) to block the IPyA route of auxin biosynthesis and to ensure that most if not all auxin in the heat-treated plants is made via the transgenic bacterial iaaM/iaaH pathway (Figure 1B). In the presence of the inhibitors, the roots of transgenic plants that received no heat shock or had auxin biosynthesis induced only in the aerial parts, like WT plants receiving the root heat shock but not harboring the auxin inducible system, lost their root meristematic activity and degenerated, whereas the heat-treated roots of transgenic plants retained healthy meristems (Figures 1B and S1D). Thus, shoot-derived auxin alone cannot support the root stem cell niche, and root sources of auxin are critical for maintaining the root meristem identity, consistent with prior findings (Chen et al., 2014Chen Q. Dai X. De-Paoli H. Cheng Y. Takebayashi Y. Kasahara H. Kamiya Y. Zhao Y. Auxin overproduction in shoots cannot rescue auxin deficiencies in Arabidopsis roots.Plant Cell Physiol. 2014; 55: 1072-1079Crossref PubMed Scopus (142) Google Scholar). Next, we applied exogenous IAA to the shoots of wei8 tar2 seedlings and examined the fate of the root meristems (Figure 1C). Unlike mock-treated plants, double mutants treated on the shoot with IAA formed several lateral and adventitious roots (Figures 1C and S1E), indicating that externally supplied auxin did move down the hypocotyl and the root. Nonetheless, the primary root meristems of plants treated with IAA on the shoot lost their stem cell identity and differentiated (Figure 1C) despite repeated application of IAA. Importantly, not only the primary roots but also the later emerging lateral and adventitious root meristems degenerated (Figures 1C and S1E), again confirming that auxin production in the root is necessary for supporting a healthy root meristem and that shoot-derived auxin, although capable of inducing new roots, is not sufficient to keep root stem cells functional. Thus, the long-distance phloem-based auxin transport from the shoot previously implicated in adventitious and lateral root emergence (Swarup et al., 2008Swarup K. Benková E. Swarup R. Casimiro I. Péret B. Yang Y. Parry G. Nielsen E. De Smet I. Vanneste S. et al.The auxin influx carrier LAX3 promotes lateral root emergence.Nat. Cell Biol. 2008; 10: 946-954Crossref PubMed Scopus (567) Google Scholar, Overvoorde et al., 2010Overvoorde P. Fukaki H. Beeckman T. Auxin control of root development.Cold Spring Harb. Perspect. Biol. 2010; 2: a001537Crossref PubMed Scopus (520) Google Scholar) and root growth (Fu and Harberd, 2003Fu X. Harberd N.P. Auxin promotes Arabidopsis root growth by modulating gibberellin response.Nature. 2003; 421: 740-743Crossref PubMed Scopus (604) Google Scholar) may not be a critical player in the generation and maintenance of a local auxin maximum in the root meristem. Root meristems of wei8 tar2 grown in media supplemented with IAA do not degenerate (Figure 2A) (Stepano}, number={3}, journal={DEVELOPMENTAL CELL}, author={Brumos, Javier and Robles, Linda M. and Yun, Jeonga and Vu, Thien C. and Jackson, Savannah and Alonso, Jose M. and Stepanova, Anna N.}, year={2018}, month={Nov}, pages={306-+} }
 @article{estrada-johnson_csukasi_pizarro_vallarino_kiryakova_vioque_merchante_brumos_medina-escobar_botella_et al._2017, title={Transcriptomic Analysis in Strawberry Fruits Reveals Active Auxin Biosynthesis and Signaling in the Ripe Receptacle (vol 8, pg 889, 2017)}, volume={8}, ISSN={["1664-462X"]}, DOI={10.3389/fpls.2017.01305}, abstractNote={[Catharina Merchante] was not included as an author in the published article. The authors apologize for this error and state that this does not change the scientific conclusions of the article in any way.}, journal={FRONTIERS IN PLANT SCIENCE}, author={Estrada-Johnson, Elizabeth and Csukasi, Fabiana and Pizarro, Carmen M. and Vallarino, Jose G. and Kiryakova, Yulia and Vioque, Amalia and Merchante, Catharina and Brumos, Javier and Medina-Escobar, Nieves and Botella, Miguel A. and et al.}, year={2017}, month={Jul} }
 @article{estrada-johnson_csukasi_pizarro_vallarino_kiryakova_vioque_brumos_medina-escobar_botella_alonso_et al._2017, title={Transcriptomic analysis in strawberry fruits reveals active auxin biosynthesis and signaling in the ripe receptacle}, volume={8}, journal={Frontiers in Plant Science}, author={Estrada-Johnson, E. and Csukasi, F. and Pizarro, C. M. and Vallarino, J. G. and Kiryakova, Y. and Vioque, A. and Brumos, J. and Medina-Escobar, N. and Botella, M. A. and Alonso, J. M. and et al.}, year={2017} }
 @article{franco-navarro_brumos_rosales_cubero-font_talon_colmenero-flores_2016, title={Chloride regulates leaf cell size and water relations in tobacco plants}, volume={67}, ISSN={["1460-2431"]}, DOI={10.1093/jxb/erv502}, abstractNote={Chloride (Cl–) is a micronutrient that accumulates to macronutrient levels since it is normally available in nature and actively taken up by higher plants. Besides a role as an unspecific cell osmoticum, no clear biological roles have been explicitly associated with Cl– when accumulated to macronutrient concentrations. To address this question, the glycophyte tobacco (Nicotiana tabacum L. var. Habana) has been treated with a basal nutrient solution supplemented with one of three salt combinations containing the same cationic balance: Cl–-based (CL), nitrate-based (N), and sulphate+phosphate-based (SP) treatments. Under non-saline conditions (up to 5mM Cl–) and no water limitation, Cl– specifically stimulated higher leaf cell size and led to a moderate increase of plant fresh and dry biomass mainly due to higher shoot expansion. When applied in the 1–5mM range, Cl– played specific roles in regulating leaf osmotic potential and turgor, allowing plants to improve leaf water balance parameters. In addition, Cl– also altered water relations at the whole-plant level through reduction of plant transpiration. This was a consequence of a lower stomatal conductance, which resulted in lower water loss and greater photosynthetic and integrated water-use efficiency. In contrast to Cl–, these effects were not observed for essential anionic macronutrients such as nitrate, sulphate, and phosphate. We propose that the abundant uptake and accumulation of Cl– responds to adaptive functions improving water homeostasis in higher plants.}, number={3}, journal={JOURNAL OF EXPERIMENTAL BOTANY}, author={Franco-Navarro, Juan D. and Brumos, Javier and Rosales, Miguel A. and Cubero-Font, Paloma and Talon, Manuel and Colmenero-Flores, Jose M.}, year={2016}, month={Feb}, pages={873–891} }
 @article{villarino_hu_manrique_flores-vergara_sehra_robles_brumos_stepanova_colombo_sundberg_et al._2016, title={Transcriptomic Signature of the SHATTERPROOF2 Expression Domain Reveals the Meristematic Nature of Arabidopsis Gynoecial Medial Domain}, volume={171}, ISSN={["1532-2548"]}, url={http://europepmc.org/abstract/med/26983993}, DOI={10.1104/pp.15.01845}, abstractNote={Plant meristems, like animal stem cell niches, maintain a pool of multipotent, undifferentiated cells that divide and differentiate to give rise to organs. In Arabidopsis (Arabidopsis thaliana), the carpel margin meristem is a vital meristematic structure that generates ovules from the medial domain of the gynoecium, the female floral reproductive structure. The molecular mechanisms that specify this meristematic region and regulate its organogenic potential are poorly understood. Here, we present a novel approach to analyze the transcriptional signature of the medial domain of the Arabidopsis gynoecium, highlighting the developmental stages that immediately proceed ovule initiation, the earliest stages of seed development. Using a floral synchronization system and a SHATTERPROOF2 (SHP2) domain-specific reporter, paired with FACS and RNA sequencing, we assayed the transcriptome of the gynoecial medial domain with temporal and spatial precision. This analysis reveals a set of genes that are differentially expressed within the SHP2 expression domain, including genes that have been shown previously to function during the development of medial domain-derived structures, including the ovules, thus validating our approach. Global analyses of the transcriptomic data set indicate a similarity of the pSHP2-expressing cell population to previously characterized meristematic domains, further supporting the meristematic nature of this gynoecial tissue. Our method identifies additional genes including novel isoforms, cis-natural antisense transcripts, and a previously unrecognized member of the REPRODUCTIVE MERISTEM family of transcriptional regulators that are potential novel regulators of medial domain development. This data set provides genome-wide transcriptional insight into the development of the carpel margin meristem in Arabidopsis.}, number={1}, journal={PLANT PHYSIOLOGY}, author={Villarino, Gonzalo H. and Hu, Qiwen and Manrique, Silvia and Flores-Vergara, Miguel and Sehra, Bhupinder and Robles, Linda and Brumos, Javier and Stepanova, Anna N. and Colombo, Lucia and Sundberg, Eva and et al.}, year={2016}, month={May}, pages={42–61} }
 @article{merchante_brumos_yun_hu_spencer_enriquez_binder_heber_stepanova_alonso_2015, title={Gene-Specific Translation Regulation Mediated by the Hormone-Signaling Molecule EIN2}, volume={163}, ISSN={["1097-4172"]}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-84948814371&partnerID=MN8TOARS}, DOI={10.1016/j.cell.2015.09.036}, abstractNote={The central role of translation in modulating gene activity has long been recognized, yet the systematic exploration of quantitative changes in translation at a genome-wide scale in response to a specific stimulus has only recently become technically feasible. Using the well-characterized signaling pathway of the phytohormone ethylene and plant-optimized genome-wide ribosome footprinting, we have uncovered a molecular mechanism linking this hormone’s perception to the activation of a gene-specific translational control mechanism. Characterization of one of the targets of this translation regulatory machinery, the ethylene signaling component EBF2, indicates that the signaling molecule EIN2 and the nonsense-mediated decay proteins UPFs play a central role in this ethylene-induced translational response. Furthermore, the 3′UTR of EBF2 is sufficient to confer translational regulation and required for the proper activation of ethylene responses. These findings represent a mechanistic paradigm of gene-specific regulation of translation in response to a key growth regulator.}, number={3}, journal={CELL}, author={Merchante, Catharina and Brumos, Javier and Yun, Jeonga and Hu, Qiwen and Spencer, Kristina R. and Enriquez, Paul and Binder, Brad M. and Heber, Steffen and Stepanova, Anna N. and Alonso, Jose M.}, year={2015}, month={Oct}, pages={684–697} }
 @article{brumos_alonso_stepanova_2014, title={Genetic aspects of auxin biosynthesis and its regulation}, volume={151}, ISSN={["1399-3054"]}, url={http://www.scopus.com/inward/record.url?eid=2-s2.0-84898468296&partnerID=MN8TOARS}, DOI={10.1111/ppl.12098}, abstractNote={Auxin is an essential plant hormone that controls nearly every aspect of a plant's life, from embryo development to organ senescence. In the last decade the key genes involved in auxin transport, perception, signaling and response have been identified and characterized, but the elucidation of auxin biosynthesis has proven to be especially challenging. In plants, a significant amount of indole-3-acetic acid (IAA), the predominant biologically active form of auxin, is synthesized via a simple two-step route where indole-3-pyruvic acid (IPyA) produced from l-tryptophan by tryptophan aminotransferases (TAA1/TAR) is converted to IAA by the YUC family of flavin monooxygenases. The TAA1/TAR and YUC gene families constitute the first complete auxin biosynthetic pathway described in plants. Detailed characterization of these genes' expression patterns suggested a key role of local auxin biosynthesis in plant development. This has prompted an active search for the molecular mechanisms that regulate the spatiotemporal activity of the IPyA route. In addition to the TAA1/TAR and YUC-mediated auxin biosynthesis, several alternative routes of IAA production have been postulated to function in plants, but their biological significance is yet to be demonstrated. Herein, we take a genetic perspective to describe the current view of auxin biosynthesis and its regulation in plants, focusing primarily on Arabidopsis.}, number={1}, journal={PHYSIOLOGIA PLANTARUM}, author={Brumos, Javier and Alonso, Jose M. and Stepanova, Anna N.}, year={2014}, month={May}, pages={3–12} }
 @article{he_brumos_li_ji_ke_gong_zeng_li_zhang_an_et al._2011, title={A Small-Molecule Screen Identifies l-Kynurenine as a Competitive Inhibitor of TAA1/TAR Activity in Ethylene-Directed Auxin Biosynthesis and Root Growth in Arabidopsis}, volume={23}, ISSN={1040-4651 1532-298X}, url={http://dx.doi.org/10.1105/tpc.111.089029}, DOI={10.1105/tpc.111.089029}, abstractNote={The interactions between phytohormones are crucial for plants to adapt to complex environmental changes. One example is the ethylene-regulated local auxin biosynthesis in roots, which partly contributes to ethylene-directed root development and gravitropism. Using a chemical biology approach, we identified a small molecule, l-kynurenine (Kyn), which effectively inhibited ethylene responses in Arabidopsis thaliana root tissues. Kyn application repressed nuclear accumulation of the ETHYLENE INSENSITIVE3 (EIN3) transcription factor. Moreover, Kyn application decreased ethylene-induced auxin biosynthesis in roots, and TRYPTOPHAN AMINOTRANSFERASE OF ARABIDOPSIS1/TRYPTOPHAN AMINOTRANSFERASE RELATEDs (TAA1/TARs), the key enzymes in the indole-3-pyruvic acid pathway of auxin biosynthesis, were identified as the molecular targets of Kyn. Further biochemical and phenotypic analyses revealed that Kyn, being an alternate substrate, competitively inhibits TAA1/TAR activity, and Kyn treatment mimicked the loss of TAA1/TAR functions. Molecular modeling and sequence alignments suggested that Kyn effectively and selectively binds to the substrate pocket of TAA1/TAR proteins but not those of other families of aminotransferases. To elucidate the destabilizing effect of Kyn on EIN3, we further found that auxin enhanced EIN3 nuclear accumulation in an EIN3 BINDING F-BOX PROTEIN1 (EBF1)/EBF2-dependent manner, suggesting the existence of a positive feedback loop between auxin biosynthesis and ethylene signaling. Thus, our study not only reveals a new level of interactions between ethylene and auxin pathways but also offers an efficient method to explore and exploit TAA1/TAR-dependent auxin biosynthesis.}, number={11}, journal={The Plant Cell}, publisher={American Society of Plant Biologists (ASPB)}, author={He, Wenrong and Brumos, Javier and Li, Hongjiang and Ji, Yusi and Ke, Meng and Gong, Xinqi and Zeng, Qinglong and Li, Wenyang and Zhang, Xinyan and An, Fengying and et al.}, year={2011}, month={Nov}, pages={3944–3960} }