A tetraspanin gene regulating auxin response and affecting orchid perianth size and various plant developmental processes

doi:10.1002/pld3.157

. 2019 Aug 5;3(8):e00157.

doi: 10.1002/pld3.157. eCollection 2019 Aug.

A tetraspanin gene regulating auxin response and affecting orchid perianth size and various plant developmental processes

Wei-Hao Chen¹, Wei-Han Hsu¹, Hsing-Fun Hsu¹, Chang-Hsien Yang^{1

2}

Affiliations

¹ Institute of Biotechnology National Chung Hsing University Taichung Taiwan, ROC.
² Advanced Plant Biotechnology Center National Chung Hsing University Taichung Taiwan, ROC.

PMID: 31406958
PMCID: PMC6680136
DOI: 10.1002/pld3.157

A tetraspanin gene regulating auxin response and affecting orchid perianth size and various plant developmental processes

Wei-Hao Chen et al. Plant Direct. 2019.

. 2019 Aug 5;3(8):e00157.

doi: 10.1002/pld3.157. eCollection 2019 Aug.

Authors

Wei-Hao Chen¹, Wei-Han Hsu¹, Hsing-Fun Hsu¹, Chang-Hsien Yang^{1

2}

Affiliations

¹ Institute of Biotechnology National Chung Hsing University Taichung Taiwan, ROC.
² Advanced Plant Biotechnology Center National Chung Hsing University Taichung Taiwan, ROC.

PMID: 31406958
PMCID: PMC6680136
DOI: 10.1002/pld3.157

Abstract

The competition between L (lip) and SP (sepal/petal) complexes in P-code model determines the identity of complex perianth patterns in orchids. Orchid tetraspanin gene Auxin Activation Factor (AAF) orthologs, whose expression strongly correlated with the expansion and size of the perianth after P code established, were identified. Virus-induced gene silencing (VIGS) of OAGL6-2 in L complex resulted in smaller lips and the down-regulation of Oncidium OnAAF. VIGS of PeMADS9 in L complex resulted in the enlarged lips and up-regulation of Phalaenopsis PaAAF. Furthermore, the larger size of Phalaenopsis variety flowers was associated with higher PaAAF expression, larger and more cells in the perianth. Thus, a rule is established that whenever bigger perianth organs are made in orchids, higher OnAAF/PaAAF expression is observed after their identities are determined by P-code complexes. Ectopic expression Arabidopsis AtAAF significantly increased the size of flower organs by promoting cell expansion in transgenic Arabidopsis due to the enhancement of the efficiency of the auxin response and the subsequent suppression of the jasmonic acid (JA) biosynthesis genes (DAD1/OPR3) and BIGPETAL gene during late flower development. In addition, auxin-controlled phenotypes, such as indehiscent anthers, enhanced drought tolerance, and increased lateral root formation, were also observed in 35S::AtAAF plants. Furthermore, 35S::AtAAF root tips maintained gravitropism during auxin treatment. In contrast, the opposite phenotype was observed in palmitoylation-deficient AtAAF mutants. Our data demonstrate an interaction between the tetraspanin AAF and auxin/JA that regulates the size of flower organs and impacts various developmental processes.

Keywords: Arabidopsis thaliana; auxin response; orchids; perianth; tetraspanin.

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Conflict of interest statement

The authors declare no conflict of interest associated with the work described in this manuscript.

Figures

**Figure 1**
Functional analysis of *OnAAF* and *PaAAF* in *Oncidium* and *Phalaenopsis* orchids. (a) Total RNA samples isolated from the lips (L), petals (P), dorsal sepals (DS), and lateral sepals (LS) of mature *Oncidium* flowers were used as templates to detect the expression of *OnAAF* by quantitative real‐time PCR. (b) Detection of *OAGL6‐2* and *OnAAF* expression in the lips of *Oncidium* floral bud (FB), open flower (OF), and mature flower (MF). (c) The flowers of *Oncidium* Lemon Heart peloric mutant (Trilips) with two petals transformed into lips (left), the *OAGL6‐2* VIGS flower (right) containing green sepal/petal‐like sectors in the lips (arrow), which are smaller than those in the wild‐type control (Mock, middle). Bar = 10 mm. Top and bottom rows indicate the adaxial and abaxial side of the flower, respectively. (d) Detection of *OnAAF* expression in L, P, DS, and LS of mature flowers of *Oncidium* Lemon Heart peloric mutant (Trilips). (e) *OnAAF* expression was higher and promoted more cell division/expansion in lips than sepals/petals, resulting in the production of larger lips than sepals/petals in *Oncidium* orchids. (f) Detection of *OAGL6‐2* and *OnAAF* expression in the lips of *OAGL6‐2* VIGS (O6‐2‐V‐1 and 2) and wild‐type control (Mock) flowers of *Oncidium* Lemon Heart. (g) The flower of *PeMADS9* (*OAGL6‐2* ortholog) VIGS *Phalaenopsis* Sogo Yukidian “V3” (Pe9‐VIGS, right) contains lips, which are larger and more spread out than in the wild‐type control flower (Mock, left) Bar = 20 mm. (h) Detection of *PaAAF* expression in lips (Lip) and P of *Phalaenopsis* Sogo Yukidian “V3” FB and OF. (i) The front lobe (L–f) and side lobe (L‐s) of the lips from (g). Bar = 10 mm. (j) Detection of *PeMADS9* (*PeM9*) and *PaAAF* expression in lips of *PeMADS9* VIGS (PM9‐V) and wild‐type control (Mock) flowers of *Phalaenopsis* Sogo Yukidian “V3.” (k) The flowers of a *Phalaenopsis* peloric mutant (Big‐Lip) have much larger sepal/petal‐like L. (l) Detection of *PaAAF* expression in L, P, DS, and LS from the Big‐Lip mutant flower in (k). (m) Higher *PaAAF* expression promoted greater cell division/expansion in sepals/petals than in lips, resulting in the production of larger petals than lips in *Phalaenopsis* orchids. (n) Two varieties of *Phalaenopsis* orchids with relatively large (P. Red Bell) and small (P. Gold Diamond) mature flower sizes. Bar = 20 mm. (o) The size comparison of the P of P. Red Bell (RB) and P. Gold Diamond (GD) from (n). (p) The comparison of the epidermal cell size in the petals of P. Red Bell (RB) and P. Gold Diamond (GD) from (n). (q, r) SEM of the epidermal cells in the petals of P. Red Bell (q) and P. Gold Diamond (r) from (n). Bar = 100 μm. (s) The comparison of the total cell number in the petals of P. Red Bell (RB) and P. Gold Diamond (GD) from (n). (t) Detection of *PaAAF* expression in P. Red Bell (RB) and P. Gold Diamond (GD) FB, OF, and MF

**Figure 2**
Analysis of the gene expression, protein localization, and palmitoylation for *AtAAF* in *Arabidopsis*. (a) The detection of *AtAAF* expression at 7 days after germination (DAG), 14 DAG, roots (Rt), rosette leaves (RL), cauline leaves (CL), floral buds (FB), and siliques (Sl). (b) The detection of *AtAAF* expression in sepal, petal, stamen, and carpel of stages 11 and 14 Arabidopsis flowers. (c) GUS staining pattern in floral buds (fb), mature flower (mf), and silique (sil) from an AtAAF::*GUS* transgenic plant. Bar = 1 mm. (d–f) GUS was detected in sepals (s), petals (p), and anther (an) of stage 10 (d) AtAAF::*GUS* flowers. GUS activity decreased in s and p and was absent in the anther after stage 12 (e, f). GUS was detected in ovules (o) after pollination (f). c, carpel. Bar = 1 mm. (g, h) Transient expression of 35S::*GFP* and 35S::*AtAAF*+*GFP* in tobacco cells. AtAAF+GFP fusion protein accumulated at the plasma membrane (h) whereas GFP protein accumulated in the cytosol (g). Bar = 30 μm. (i) Assaying palmitoylation of AtAAF and dominant negative mutant AtAAF^palm. Proteins were prepared from the 35S::*AtAAF*+*GFP* and 35S::*AtAAF^palm* +*GFP* plants by the biotin switch palmitoylation assay. Western blot analysis of proteins with the presence (+) and absence (−) of hydroxylamine treatment using a GFP antibody

**Figure 3**
Functional analysis of flower and seed size for 35S::*AtAAF* and 35S::*AtAAF^palm Arabidopsis*. (a, b) The flower (a) and petals (b) of 35S::*AtAAF* (left), wild‐type (middle), and 35S::*AtAAF^palm* (right) Arabidopsis. Bar = 1 mm. (c) Size comparison of the petals from 35S::*AtAAF* (*AtAAF*), WT, and 35S::*AtAAF^palm* (palm) Arabidopsis. Petals from three flowers for each plant (*AtAAF*, WT, and palm) were used to measure the average size. The size of the wild‐type petals is set at 100%. (d, e) Comparison of total cell number (d) and the epidermal cell size (e) in petals from 35S::*AtAAF* (*AtAAF*), wild‐type (WT), and 35S::*AtAAF^palm* (palm) Arabidopsis. (f–k) Confocal laser scanning microscopy of the epidermal cells in the petals from 35S::*AtAAF* (f, g), WT (h, i), and 35S::*AtAAF^palm* (j, k) flowers. (g), (i), and (k) are close‐ups of (f), (h), and (j), respectively. Bar = 20 μm in (f, h, j) and 5 μm in (g, i, k). (l) The mature siliques of 35S::*AtAAF* (right) and wild‐type (WT, left) Arabidopsis. Bar = 5 mm. (m–o) The seeds of 35S::*AtAAF* (m), WT (n), and 35S::*AtAAF^palm* (o) Arabidopsis. Bar = 0.2 mm. (p) Comparison of the weight for 1,000 seeds from 35S::*AtAAF* (*AtAAF*), WT, and 35S::*AtAAF^palm* (palm) Arabidopsis. (q) Detection of *AtAAF* expression for one WT and two 35S::*AtAAF* (−1, −2) plant. The asterisks in (c, d, e, p) indicate a significant difference from the WT value (*p ≤ .05, **p ≤ .01). Statistic analysis was measured by Student's t test

**Figure 4**
Phenotypic analysis of 35S::*AtAAF^palm* dominant negative mutant *Arabidopsis*. (a) Five‐week‐old 35S::*AtAAF^palm* Arabidopsis (right) produced smaller rosette leaves which showed earlier senescence (arrowed) than the wild‐type plants (left). Bar = 10 mm. (b, c) 35S::*AtAAF^palm* transgenic plants showed earlier senescence of rosette (b, right) and cauline leaves (c, right, arrow) than the wild‐type (WT, left). Bar = 5 mm. (d) Flowers from a severe 35S::*AtAAF^palm* inflorescence which showed earlier senescence than WT flowers. Bar = 1 mm. (e) Close‐up of the flowers from a severe 35S::*AtAAF^palm* inflorescence shown in (d). Bar = 1 mm. (f) Detection of expression for *AtAAF,* senescence‐related gene (*SAG12*), and the ethylene response genes (*ERF1, EDF1,* and *EDF2*) in floral buds (FB) before stage 12 from one WT plant and two severe 35S::*AtAAF^palm* plants (palm‐24 and palm‐10). Transcript levels in 35S::*AtAAF^palm* plants are presented relative to those in the wild‐type plant, which were set to 1. (g) Close‐up of the flowers from a medium–severe 35S::*AtAAF^palm‐M* inflorescence. The numbers indicate the positions of the open flowers. Bar = 1 mm. (h) Close‐up of the flowers from wild‐type (top row) and 35S::*AtAAF* (bottom row) inflorescences. The 35S::*AtAAF* flowers are clearly larger and abscised later than wild‐type flowers. The numbers indicate the positions of the open flowers. Bar = 1 mm. (i) Detection of *AtAAF* expression in FB and mature flowers (Fl) of one WT, two severe 35S::*AtAAF^palm* (palm‐10, ‐24), and one medium–severe 35S::*AtAAF^palm* (palm‐11) plants. (j) Detection of *SAG12* expression in WT and two 35S::*AtAAF* (*AtAAF‐14‐1* and *AtAAF‐14‐2*) plants

**Figure 5**
Phenotypic analysis of Arabidopsis plants ectopically expressing *AtAAF*. (a) A 35S::*AtAAF* plant (right) was sterile and produced short siliques (arrow), whereas wild‐type plants (WT, left) produced long, well‐developed siliques (arrow). Bar = 30 mm. (b) Inflorescences from a 35S::*AtAAF* plant that showed sterility with short siliques (arrow). Bar = 10 mm. (c–f) Indehiscent anthers (arrow) were observed at stage 12 in WT plants (c), stages 12 (e), and 14 (f) 35S::*AtAAF* flowers compared with stage 14 wild‐type flower (d), which showed normal anther dehiscence (arrow) and pollen (po) release. Bar = 0.5 mm. (g–j) Close‐up of stage 12 (g) wild‐type, stages 12 (i), and 14 (j) 35S::*AtAAF* anther compared with stage 14 wild‐type anther (h) by SEM, which showed normal anther dehiscence and pollen (arrow) release. Bar = 200 μm. (k–n) Close‐up of the stage 12 (k), 14 (l) wild‐type and stage 12 (m), 14 (n) 35S::*AtAAF* pollen grains by SEM. Bar = 10 µm

**Figure 6**
The analysis of drought and salt tolerance for 35S::*AtAAF* plants. (a, b) One‐week‐old wild‐type (a) and 35S::*AtAAF* (b) seedlings were tested for drought tolerance by removing them from MS medium and exposing them to a stream of air for 15, 30, 45, 60, 75, or 90 min. Bar = 5 mm. (c) The 35S::*AtAAF* (*AtAAF*) seedlings clearly withered later and lost less weight than wild‐type (WT) seedlings at 15, 30, and 60 min after drought treatment. In contrast, the 35S::*AtAAF^palm* (palm) seedlings clearly withered earlier and lost more weight than WT seedlings at 15, 30, and 60 min after drought treatment. (d) Comparison of germination for the 35S::*AtAAF* and WT seedlings grown on MS medium containing 150 mM NaCl. Bar = 10 mm. (e, f) Close‐up of the 35S::*AtAAF* (e) and WT (f) seedlings grown on MS medium containing 150 mM NaCl. Bar = 5 mm. (g) The survival rate for WT and two lines of 35S::*AtAAF (‐1‐4, ‐1‐9*) seedlings grown on MS medium containing 150 mM NaCl. (h, i) Detection of *AtAAF* expression after 15, 30, or 60 min of drought (h) or salt (i) treatment in wild‐type plants

**Figure 7**
Investigation of the relationship between *AtAAF* and Auxin response in *Arabidopsis*. (a) Detection of *GFP* expression in DR5::*GFP* and DR5::*GFP*/35S::*AtAAF* transgenic Arabidopsis after 1, 2, and 4 hr of external IAA treatment. (b) Detection of the amount of IAA in wild‐type (WT), 35S::*AtAAF* (*AAF*), and 35S::*AtAAF^palm* (palm) flower buds (FB). (c) Number of lateral roots produced in WT and 35S::*AtAAF* (*AtAAF*) Arabidopsis seedlings grown on MS medium with or without IAA/2‐NOA (auxin influx inhibitor) treatments. (d) The development of the primordia (arrowhead) for lateral roots of the WT and 35S::*AtAAF* roots of 14 DAG seedlings 18 hr post‐gravitropic induction with (d‐3 and d‐4) or without (d‐1 and d‐2) IAA treatment. Stage I (d‐1), VII (d‐2), VI (d‐3), and beyond stage VIII (d‐4) primordia of lateral roots were formed. Bar = 50 μm. (e) Root gravitropic assays for DR5::*GFP* roots with 5 days of a 90‐degree gravitropic stimulus without (mock, e‐1) or with IAA (e‐3) or 2‐NOA (e‐5) treatment. Bar = 0.5 mm. The detection of GFP in the lower (L) and upper (U) parts of the DR5::*GFP* root tips 5 hr after 90‐degree gravitropic stimulus without (mock, e‐2) or with IAA (e‐4) or 2‐NOA (e‐6) treatment. Bar = 50 μm. (f) The detection of GFP integrated intensity in lower and upper parts of the DR5::*GFP* root tips from (e‐2), (e‐4) and (e‐6). (g) Root gravitropic assays for 35S::*AtAAF*/DR5::*GFP* roots after 5 days of a 90‐degree gravitropic stimulus without mock (g‐1) or with IAA (g‐3) or 2‐NOA (g‐5) treatment. Bar = 0.5 mm. The detection of GFP in lower (L) and upper (U) parts of the 35S::*AtAAF*/DR5::*GFP* root tips 5 hr after 90‐degree gravitropic stimulus without (mock, g‐2) or with IAA (g‐4) or 2‐NOA (g‐6) treatment. Bar = 50 μm. (h) The detection of GFP integrated intensity in lower and upper parts of the 35S::*AtAAF*/DR5::*GFP* root tips from (g‐2), (g‐4), and (g‐6)

**Figure 8**
Model for the function of *AAF* orthologues in regulating auxin response and development in plants. In plants, the targeting of palmitoylated AAF proteins to the plasma membrane promotes auxin uptake and enhances (→) the auxin response. In flowers, *AAF* is more highly expressed in early than in late developmental stages (gray bar). Thus, it mainly enhances the auxin response and promotes (green arrow) cell division/expansion in the flower organs at an early stage. Ectopic expression of *AAF* extends its affect to the whole flower and results in an increase in the size of the flower organs. By contrast, a palmitoylation‐deficient mutant of AAF reduces ([]) the auxin response and alters its ability to promote cell division/expansion in early flowering stages resulting in a decrease in flower organ size. In addition, the enhancement of the auxin response by ectopic expression of *AAF* could suppress anther dehiscence during whole flower development by suppressing the expression of *MYB26*/*NST1/2, DAD1*/*OPR3,* and JA activity (which also causes the suppression of the *BPEp* and resulted in the expansion of the flower organs). The enhancement of the auxin response by AAF also suppresses ethylene signaling and organ senescence, promotes drought/salt tolerance and lateral root formation, and retains root tip gravitropism in plants. Dominant negative mutation of *AAF* suppresses auxin response and causes the opposite effect on the processes described above

formula image — **Figure 8**
Model for the function of *AAF* orthologues in regulating auxin response and development in plants. In plants, the targeting of palmitoylated AAF proteins to the plasma membrane promotes auxin uptake and enhances (→) the auxin response. In flowers, *AAF* is more highly expressed in early than in late developmental stages (gray bar). Thus, it mainly enhances the auxin response and promotes (green arrow) cell division/expansion in the flower organs at an early stage. Ectopic expression of *AAF* extends its affect to the whole flower and results in an increase in the size of the flower organs. By contrast, a palmitoylation‐deficient mutant of AAF reduces ([]) the auxin response and alters its ability to promote cell division/expansion in early flowering stages resulting in a decrease in flower organ size. In addition, the enhancement of the auxin response by ectopic expression of *AAF* could suppress anther dehiscence during whole flower development by suppressing the expression of *MYB26*/*NST1/2, DAD1*/*OPR3,* and JA activity (which also causes the suppression of the *BPEp* and resulted in the expansion of the flower organs). The enhancement of the auxin response by AAF also suppresses ethylene signaling and organ senescence, promotes drought/salt tolerance and lateral root formation, and retains root tip gravitropism in plants. Dominant negative mutation of *AAF* suppresses auxin response and causes the opposite effect on the processes described above

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References

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1. Azooz, M. M. , Shaddad, M. A. , & Abdel‐Latef, A. A. (2004). Leaf growth and K+/Na+ ratio as an indication of the salt tolerance of three sorghum cultivars grown under salinity stress and IAA treatment. Acta Agronomica Hungarica, 52, 287–296.
1. Benková, E. , Michniewicz, M. , Sauer, M. , Teichmann, T. , Seifertová, D. , Jürgens, G. , & Friml, J. (2003). Local, efflux‐dependent auxin gradients as a common module for plant organ formation. Cell, 115, 591–602. 10.1016/S0092-8674(03)00924-3 - DOI - PubMed

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[1] Alexander, M. P. (1969). Differential staining of aborted and nonaborted pollen. Stain Technology, 44, 117–122. 10.3109/10520296909063335 - DOI - PubMed

[2] Alexander, M. P. (1969). Differential staining of aborted and nonaborted pollen. Stain Technology, 44, 117–122. 10.3109/10520296909063335 - DOI - PubMed

[3] Alonso, J. M. , Stepanova, A. N. , Leisse, T. J. , Kim, C. J. , Chen, H. , Shinn, P. , … Ecker, J. R. (2003). Genome‐wide insertional mutagenesis of Arabidopsis thaliana . Science, 301, 653–657. 10.1126/science.1086391 - DOI - PubMed

[4] Alonso, J. M. , Stepanova, A. N. , Leisse, T. J. , Kim, C. J. , Chen, H. , Shinn, P. , … Ecker, J. R. (2003). Genome‐wide insertional mutagenesis of Arabidopsis thaliana . Science, 301, 653–657. 10.1126/science.1086391 - DOI - PubMed

[5] Armengot, L. , Marques‐Bueno, M. M. , & Jaillais, Y. (2016). Regulation of polar auxin transport by protein and lipid kinases. Journal of Experimental Botany, 67, 4015–4037. 10.1093/jxb/erw216 - DOI - PMC - PubMed

[6] Armengot, L. , Marques‐Bueno, M. M. , & Jaillais, Y. (2016). Regulation of polar auxin transport by protein and lipid kinases. Journal of Experimental Botany, 67, 4015–4037. 10.1093/jxb/erw216 - DOI - PMC - PubMed

[7] Azooz, M. M. , Shaddad, M. A. , & Abdel‐Latef, A. A. (2004). Leaf growth and K+/Na+ ratio as an indication of the salt tolerance of three sorghum cultivars grown under salinity stress and IAA treatment. Acta Agronomica Hungarica, 52, 287–296.

[8] Azooz, M. M. , Shaddad, M. A. , & Abdel‐Latef, A. A. (2004). Leaf growth and K+/Na+ ratio as an indication of the salt tolerance of three sorghum cultivars grown under salinity stress and IAA treatment. Acta Agronomica Hungarica, 52, 287–296.

[9] Benková, E. , Michniewicz, M. , Sauer, M. , Teichmann, T. , Seifertová, D. , Jürgens, G. , & Friml, J. (2003). Local, efflux‐dependent auxin gradients as a common module for plant organ formation. Cell, 115, 591–602. 10.1016/S0092-8674(03)00924-3 - DOI - PubMed

[10] Benková, E. , Michniewicz, M. , Sauer, M. , Teichmann, T. , Seifertová, D. , Jürgens, G. , & Friml, J. (2003). Local, efflux‐dependent auxin gradients as a common module for plant organ formation. Cell, 115, 591–602. 10.1016/S0092-8674(03)00924-3 - DOI - PubMed

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A tetraspanin gene regulating auxin response and affecting orchid perianth size and various plant developmental processes

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A tetraspanin gene regulating auxin response and affecting orchid perianth size and various plant developmental processes

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Abstract

Conflict of interest statement

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Abstract

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